ArticlePDF Available

New evidence that the MHC influences odor perception in humans: A study with 58 Southern Brazilian students



Increasing evidence suggests a correlation between mate choice, odor preference, and genetic similarity at the Major Histocompatibility Complex (MHC) in a variety of animals, including our species. The MHC is a highly polymorphic group of genes that play an important role in the immunological self/nonself recognition. Its products have been reported to take part on the variety of compounds and reactions that together build an individual's body odor. It has been suggested, therefore, that animals use body odor as a guide to identify possible mates as MHC-similar or MHC-dissimilar from their own genotype. Preference for a MHC-dissimilar partner enhances MHC heterozygosity of an individual's offspring. The possible adaptive advantages are clear: it is a mechanism of avoiding inbreeding and MHC-heterozygous offspring may have enhanced immunocompetence. The aim of this study was to search, in our species, new evidence on the correlation between specificities at HLA-A and HLA-B and assessments of pleasantness regarding specific body odors. HLA is the name for the human MHC. Four olfactory sessions were performed with 58 young Southern Brazilian students, in order to investigate whether assessments of pleasantness of body odors from individuals correlate to a person's HLA phenotype. Body odors were collected via sweat and urine from all participants. Women smelled and scored all male odor samples and men did the same with all female samples. We found a significant correlation only when female smellers evaluated male sweat odors.
New evidence that the MHC influences odor perception in humans:
a study with 58 Southern Brazilian students
Pablo Sandro Carvalho Santos, Juliano Augusto Schinemann,
Juarez Gabardo, Maria da Grac¸a Bicalho*
LIGH—Laborato´rio de Imunogene´tica e Histocompatibilidade, Departamento de Gene´tica, Setor de Cieˆncias Biolo´ gicas,
Centro Polite´cnico da Universidade Federal do Parana´ , Jardim das Ame´ ricas, Caixa Postal 19071, CEP: 81.530-990 Curitiba, Parana´, Brazil
Received 2 February 2004; revised 1 June 2004; accepted 5 November 2004
Available online 2 February 2005
Increasing evidence suggests a correlation between mate choice, odor preference, and genetic similarity at the Major Histocompatibility
Complex (MHC) in a variety of animals, including our species. The MHC is a highly polymorphic group of genes that play an important role
in the immunological self/nonself recognition. Its products have been reported to take part on the variety of compounds and reactions that
together build an individual’s body odor. It has been suggested, therefore, that animals use body odor as a guide to identify possible mates as
MHC-similar or MHC-dissimilar from their own genotype. Preference for a MHC-dissimilar partner enhances MHC heterozygosity of an
individual’s offspring. The possible adaptive advantages are clear: it is a mechanism of avoiding inbreeding and MHC-heterozygous
offspring may have enhanced immunocompetence. The aim of this study was to search, in our species, new evidence on the correlation
between specificities at HLA-A and HLA-B and assessments of pleasantness regarding specific body odors. HLA is the name for the human
MHC. Four olfactory sessions were performed with 58 young Southern Brazilian students, in order to investigate whether assessments of
pleasantness of body odors from individuals correlate to a person’s HLA phenotype. Body odors were collected via sweat and urine from all
participants. Women smelled and scored all male odor samples and men did the same with all female samples. We found a significant
correlation only when female smellers evaluated male sweat odors.
D2004 Elsevier Inc. All rights reserved.
Keywords: HLA; Mate choice; MHC; Negative assortative mating; Odors; Reproductive behavior; Sex attractants; Smell
Since Yamazaki and his colleagues published their
seminal paper in 1976, increasing interest has been directed
to the influence of the Major Histocompatibility Complex
(MHC) on mating preferences. Yamazaki and his colleagues
observed MHC-based disassortative mating preferences
mediated by odor in house mice, Mus musculus domesticus
(Yamazaki et al., 1976). Since then, several studies have
been published showing that the MHC is, somehow, a
source of unique personal odor, which influences individual
recognition and/or mating preferences in rodents (Beau-
champ et al., 1988; Eklund, 1997; Penn and Potts, 1998;
Yamazaki et al., 1978), in humans (Jacob et al., 2002; Ober
et al., 1997; Wedekind et al., 1995), in fish (Landry et al.,
2001; Milinski, 2003; Olse´n et al., 1998), and recently in
sand lizards (Olsson et al., 2003) and in birds (Freeman-
Gallant et al., 2003).
Brown (1979) refers very properly to individual odors
from mammals as bolfactory fingerprintsQ, as they seem to
enable detailed identification among individuals, conspecific
and not. In the same work, Brown proposes that mammals use
their body odor in order to provide a variety of information,
such as sex, species, age class (infant, juvenile, or adult),
colony or family membership, reproductive status (rut or
heat), social status, stress (fear or alarm state), maternal
status (pregnancy/lactation), and individual identity.
Implication of MHC genes in kin recognition has been
described in mice (Manning et al., 1992) and at least one
0018-506X/$ - see front matter D2004 Elsevier Inc. All rights reserved.
* Corresponding author. Fax: +55 41 2662042.
E-mail address: (M. da Grac¸a Bicalho).
Hormones and Behavior 47 (2005) 384 388
relatively recent report (Lewis, 1998) relates these genes
with the evolution of kin altruism.
One of the first works of this kind concerning humans
was carried out by Wedekind et al. (1995). They found that
women tend to prefer body odor from individuals carrying a
different HLA-genotype (the human MHC is called HLA,
Human Leukocyte Antigen). On their review of studies on
MHC-dependent mating preferences in many species, Penn
and Potts (1999) described three possible adaptive signifi-
cances of this phenomenon, which we summarize in two:
first, MHC-disassortative mating patterns produce MHC-
heterozygous offspring, which may have enhanced immu-
nocompetence and be more resistant against pathogens.
Second, MHC-disassortative mating preferences may help
avoiding inbreeding.
Although many works agree with the possible benefits of
maximizing MHC-heterozygosity, recent researches suggest
a different approach: there might be an optimum, inter-
mediate degree of MHC-heterozygosity, which would bring
more fitness than the strongest possible heterozygosity. One
example is the work by Milinski (2003), who studied a
species of fish, the three-spined Stickleback, and found that
female sticklebacks tend to optimize (and not to maximize)
the MHC-heterozygosity of offspring through mate choice.
Milinski (2003) demonstrated that offspring with an
intermediate number of different MHC alleles are fitter than
both strongly homozygous and strongly heterozygous
individuals. Jacob et al. (2002) came to comparable findings
in a very elegant work that had humans as subjects: their
study leads to the conclusion that women tend to prefer the
smell of a man that has an intermediate number of HLA
matches to their own, rather than the smell of men carrying
HLA alleles that are too similar or too different from theirs.
The MHC is a large chromosomal region containing
many linked, highly polymorphic genes that play a central
role in controlling immunological self/nonself recognition
(Klein, 1986), and its genetic diversity seems to be its major
feature. Many theories have been sought to explain how an
individual’s MHC-genotype shapes its body odors. In
another review, Penn and Potts summarized five hypotheses
explaining the possible ways that this could happen,
although none are proven to date (see Penn and Potts,
1998 for details).
An impressive number of the functional HLA genes are
related to the immune system, but many other HLA genes
(or HLA-linked) are not. Examples are some human
olfactory receptor-like genes, which have been reported to
be HLA-linked (Eklund et al., 2000; Fan et al., 1996;
Ziegler et al., 2000). Ziegler et al. (2000) demonstrated the
existence of more than thirty olfactory receptor genes
located at the HLA class I region, in the immediate vicinity
of the HLA-F locus. As Eklund et al. (2000) put it, HLA-
linked olfactory receptor genes provide a potential mecha-
nism for detecting HLA-specific odors.
The main goal of this work was to test whether HLA-A
and HLA-B specificities correlate to one individual’s
perception of a specific body odor or not. Moreover, we
aimed to test whether we were able to reproduce the main
findings of Wedekind et al. (1995) assessing only HLA class
I loci and using an alternative methodological approach.
Although it has been reported that the use of contra-
ceptives might mask female odor perception, we did not
distinguish between, in our statistical analysis, women who
were taking oral contraceptives from women who were not.
We found, however, a significant correlation between HLA
phenotypes from female smellers and from male represented
by sweat odor samples. We observed that when women
evaluated the smell of sweat coming from males, the level of
difficulty in deciding whether a sample was bpleasantQor
bunpleasantQincreased significantly with the increased level
of HLA-similarities between smeller and odor donor. We
did not observe a significant correlation when female
smellers scored male urine samples. No significant correla-
tion was observed when male smellers scored both kinds of
female samples (sweat and urine) either. Men neither dlikedT
nor ddislikedTa smell that was in some way related to a
woman’s HLA phenotype. Women seemed to do so, but
only when the odor sample was collected through sweat.
A total of 58 Southern Brazilian students (29 male and 29
female) self-reported heterosexual from the Federal Uni-
versity of Parana´, city of Curitiba, took part in this study.
Curitiba is the capital city of the Southern Brazilian Federal
State of Parana´, with approximately 1.5 million inhabitants.
Mainly Germans, Italians, Polish, and Portuguese formed its
population, since the official immigration policy was
established in the XIX century. Nine female participants
(31.03% of female subjects) were taking oral contraceptives.
Participants were aged between 18 and 27 years (average
age 19.76 years). None of them had relatives taking part in
the study. All participants were informed about the goal of
this investigation: a search for a correlation between their
odor perception and their HLA phenotypes, using an
analysis of HLA matches and mismatches between smellers
and odor donors. All subjects agreed to follow the necessary
restrictions on their personal routine (described below)
throughout the time for preparation and performance of the
olfactory sessions. Ethical approval for this study was
obtained from the Ethics Committee at Hospital de Clı´nicas,
and informed consent to participate in the study was
obtained from all individuals.
On August 1999, all participants had their HLA-A and
HLA-B serologically typed at the Laborato´rio de Imunoge-
ne´tica e Histocompatibilidade—LIGH, at the Federal Uni-
P. Sandro Carvalho Santos et al. / Hormones and Behavior 47 (2005) 384–388 385
versity of Parana´. Phenotypings were performed using
peripheral blood lymphocytes and a ONE LAMBDA
Special Monoclonal Typing Tray Set—SMT144A. The
privacy of the personal data of all participants was assured
by the laboratory named above.
Preparation for the olfactory sessions
On May 2000, each person was given a necklace with a
sachet that was made of absorbent cotton. The sachets were
manufactured by covering and sewing a 4 cm 4cm
0.5 cm patch of 100% untreated cotton with a cotton gauze.
All subjects carried the sachet on their breasts, at the height
of the sternum (an area of high perspiration), for 5 days,
aiming the absorbance of body odors through sweat. During
this time, they were allowed to use only neutral personal
hygiene products, all from the same lot provided by a
Brazilian cosmetics company. Participants were asked to
avoid other products that could mask their natural odors,
such as cigarettes, chewing gums, alcohol, and all strong
natural or artificial flavored food. They were allowed to take
a shower, but not to bathe, once in a day, using the provided
personal hygiene products and after placing their sachets in
a closed plastic recipient that had been given to each
participant for that purpose. After 1 h, they should be
wearing the necklace with the sachet again. Sexual contact
should be avoided. After the five preparation days, all
sachets were collected and put in sealed plastic bags. All
bags were identified with a code. The first urine of the fifth
preparation day from each participant was also collected.
Stripes of absorbent paper were put in contact with each
urine sample so that each stripe represented one individual’s
urine sample. Stripes were put in sealed plastic bags that
were also identified with a code. The olfactory tests began
on the day after the fifth preparation day.
The olfactory sessions
Tab le 1 summarizes the four olfactory sessions, which
were performed in 2 days: sessions 1 and 2 on the first day
and sessions 3 and 4 on the day after. Participants received
on both days a worksheet in which they evaluated the odor
from each sample using three possible categories: pleasant,
indifferent, or unpleasant. Before each evaluation, they
briefly sniffed a sample of coffee powder that had been
given to each of them, so that they could avoid misinter-
pretation between the odors from different samples.
Participants were aware that they were scoring samples
from individuals from the opposite sex, but they were
ignorant of the source person of each odor sample.
Statistical analysis
At each of the two HLA loci studied, there was a
possibility of up to two allele matches, for a maximum of
four matches.
We compared male HLA-A and HLA-B phenotypes with
female HLA-A and HLA-B phenotypes and stratified the
possible matches considering all possible male/female
combinations in 4 categories as follows:
0 —When a pair shared no HLA specificities.
1 —When a pair shared 1 HLA specificity.
2 —When a pair had 2 HLA specificities in common.
3 —When a pair had 3 HLA specificities in common.
The situation in which a pair shared all 4 specificities
(HLA identicals) was not observed.
Chi-square tests (independence and goodness-of-fit)
were used for all comparisons. Data analysis was performed
using the electronic tools MICROSTAT (Ecosoft, Inc.) and
EpiCalc 2000 (v.1.02, Joe Gilman and Mark Myatt, 1998,
Brixton Books).
Results and discussion
Table 2 displays the results of the first olfactory session,
in which female participants scored the sachets that had
been worn by male subjects.
Out of the four olfactory sessions, the one shown on
Table 2 was the only session in which we observed a
significant correlation (v
= 14.37; df =4;P= 0.0062)
between degrees of HLA-similarities and assessments of
The total number of scorings on Table 2 is 838, and not
841, as it would be expected (29 smellers 29 donors)
because three female smellers failed to score one different
sachet each. All three blostQsmeller/donor pairs belonged to
the category bzero matchesQ.
Due to the small number of smeller/donor pairs belong-
ing to the category b3 matchesQ(there were 7 pairs in this
category), we decided to merge that category with its upper
immediate, the category b2 matchesQ.
Table 1
Summary of the olfactory sessions performed
Olfactory session Smellers Donors Odor
No. of
1 29 Female 29 Male Sweat 838
2 29 Male 29 Female Sweat 838
3 29 Female 29 Male Urine 837
4 27 Male 29 Female Urine 781
Number differs from 841 (29
) because three smellers failed to score one
different sample each, all belonging to the category bno matchesQ.
Number differs from 841 because three smellers failed to score one
different sample each, all belonging to the category bno matchesQ.
Number differs from 841 because four smellers failed to score one
different sample each, three in the category bno matchesQand one in the
category bone matchQ.
Number differs from 841 because two male smellers did not come to this
olfactory session and one smeller failed to score 2 urine samples, category
bone matchQ.
P. Sandro Carvalho Santos et al. / Hormones and Behavior 47 (2005) 384–388386
A preliminary analysis of the results could suggest
similar findings as those by Wedekind et al. (1995): female
smellers are more likely to find the odor of a male’s sweat
pleasant when they share less HLA specificities. This would
be, however, a misinterpretation. Chi-squared goodness-of-
fit tests were performed in each score category (shown in
Table 2), testing against null hypothesis that our data fit the
expected data. The results of the goodness-of-fit tests
indicate that the samples scored as bindifferentQare
responsible for driving the statistical association of the first
olfactory session (v
= 10.12; df =2;P= 0.0064), and not
the samples evaluated as bpleasantQ(v
= 1.46; df = 2; n.s.),
or bunpleasantQ(v
= 2.79; df = 2; n.s.).
The other three olfactory sessions showed results that,
according to our statistical analysis, correspond to a pattern
of odor assessments regarding HLA phenotypes similar to
the pattern that would be expected by chance (also shown
on Table 1). The results of the chi-squared independence
tests are for session 2 (v
= 4.632; df = 6; n.s.), 3 (v
6.308; df = 6; n.s.), and 4 (v
= 3.852; df = 6; n.s.) not
As Koelega and Kfster (1974) concluded from a series of
experiments in odor perception, our results also suggest that
men seem to be less sensitive to smelling stimuli than
The work by Herz and Inzlicht (2002) supports this view,
showing that this kind of stimulus seems to be much more
important for women than for men, when many variables for
sexual interest are compared.
Our results regarding the sweat samples are not in
agreement with the findings of Wedekind et al. (1995) and
Wedekind and Fu¨ri (1997), who found that perceived
pleasantness of body odors tend to correlate negatively
with the degree of HLA similarity between female smellers
and male sample donors. Instead, our study indicates that a
significant increase of difficulty to decide between pleasant
or unpleasant regarding sweat odors correlates positively
with the increase of HLA-class I similarities between odor
smeller and donor. Moreover, works by Wedekind et al.
(1995) and Wedekind and Fu¨ri (1997) did find an asso-
ciation when male acted as smellers, whereas we did not.
Both differences could be related to the fact that subjects in
our study were typed only for HLA class I loci. As a result,
smeller/donor pairs that we classified in the category bzero
matchesQcould actually match for one or two class II loci.
According to the review by Penn and Potts (1999), no study
demonstrating MHC-dependent mating and odor preferen-
ces had ignored MHC class II genes until that time. The
most consistent evidence linking the HLA class I region
with odor perception are works that relate olfactory receptor
genes with the HLA class I region (Eklund et al., 2000; Fan
et al., 1996; Ziegler et al., 2000). It is notable that a
significant correlation between odor perception and HLA-
similarities was observed in this work in spite of the fact that
we did not investigate HLA class II genes.
Our results (and those by Wedekind and Fu¨ ri, 1997;
Wedekind et al., 1995) differ from the findings by Jacob
et al. (2002), who reported that women prefer odors coming
from men with an boptimalQ, intermediate number of HLA
matches with their own. An important difference between
their methods (Jacob et al., 2002) and ours is that we did not
perform a preference test, whereas they did. Subjects in our
study were judging pleasantness (blikingQ), when they
scored the odor samples, while subjects in their study
(Jacob et al., 2002) were actually choosing (bwantingQ)a
specific odor. bLikingQand bwantingQare, according to the
review of Berridge and Robinson (1998), rather indepen-
dent. The paradoxical bwantingQwithout blikingQis quite
possible, as blikingQand bwantingQseem to involve different
brain substrates (Berridge and Robinson, 1998). Other
differences concerning the study design, such as the
statistical treatment of data and the selection of smellers,
make it difficult to directly compare their study (Jacob et al.,
2002) with ours.
Still, our results differ from those of Wedekind et al.
(1995) and Wedekind and Fu¨ri (1997) in that we did not
stratify, in our statistical analysis, women who were taking
oral contraceptives from women who were not. Notably, a
significant correlation was observed in spite of this fact,
which, according to Pause et al. (1996), modulates olfactory
perception. Similarly, the study by Jacob et al. (2002) found
that women can discriminate between odors from donors
with different HLA types, testing women without regard to
menstrual cycle phase.
Our results show that a significant correlation between
HLA-similarities and female odor perception takes place
even without assessing two features that are had to be
decisive on olfactory perception: HLA class II genes and
menstrual cycle phase/use of oral contraceptives.
As Wedekind and Fu¨ri (1997) put it, odor preferences in
humans appear to be context-dependent. Personal history,
hormonal status, and psychological context are a few of the
possible variables that are likely to influence human
Table 2
Olfactory session 1: number of HLA matches (M) between female smellers
and male donors versus female assessments of male sweat odor
Number Score categories Total
of HLA
Pleasant* Indifferent** Unpleasant***
192 (48.24%) 82 (20.60%) 124 (31.16%) 398 (100%)
154 (43.63%) 90 (25.50%) 109 (30.88%) 353 (100%)
35 (40.23%) 34 (39.08%) 18 (20.69%) 87 (100%)
Total 381 (45.47%) 206 (24.58%) 251(29.95%) 838 (100%)
-test for independence = 14.37; df =4;P= 0.0062.
29 smellers and 29 donors involved.
29 smellers and 29 donors involved.
23 smellers and 21 donors involved.
-goodness-of-fit test in the bpleasantQcategory: v
= 1.46; df = 2; n.s.
** v
-goodness-of-fit test in category bindifferentQ:v
= 10.12; df =2;P=
*** v
-goodness-of-fit test in the bunpleasantQcategory: v
= 2.79; df =2;
P. Sandro Carvalho Santos et al. / Hormones and Behavior 47 (2005) 384–388 387
preferences. It is our understanding that in studies with
humans, we can at best conclude that HLA loci or HLA-
linked genes influence body odor production and/or per-
ception. Extrapolative considerations on human sexual
attraction or mating preferences still do not have empirical
support. In this concern, new studies with alternative
approaches need to be carried out, in order to test a broader
spectrum of different contexts that might be likely to
influence human mating behavior.
Beauchamp, G.K., Yamazaki, K., Bard, J., Boyse, E.A., 1988. Preweaning
experience in the control of mating preferences by genes in the major
histocompatibility complex of the mouse. Behav. Genet. 18, 537 547.
Berridge, K.C., Robinson, T.E., 1998. What is the role of dopamine in
reward: hedonic impact, reward learning, or incentive salience? Brain
Res. Rev. 28, 309 369.
Brown, R.E., 1979. Mammalian social odours. Adv. Stud. Behav. 10,
103 109.
Eklund, A., 1997. The effect of early experience on MHC-based mate
preferences in two B10.W strains of mice (Mus domesticus). Behav.
Ecol. 8, 630 634.
Eklund, A.C., Belchak, M.M., Lapidos, K., Raha-Chowdhury, R., Ober, C.,
2000. Polymorphisms in the HLA-linked olfactory receptor genes in the
Hutterites. Hum. Immunol. 61, 711– 717.
Fan, W., Weiwen, C., Parimoo, S., Lennon, G.G., Weissman, S.M., 1996.
Identification of seven new MHC class I region genes around the HLA-
F locus. Immunogenetics 44, 97 103.
Freeman-Gallant, C.R., Meguerdichian, M., Wheelwright, N.T., Sollecito,
S.V., 2003. Social pairing and female mating fidelity predicted by
restriction fragment length polymorphism similarity at the major
histocompatibility complex in a songbird. Mol. Ecol. 12, 3077 3083.
Herz, R.S., Inzlicht, M., 2002. Sex differences in response to physical and
social factors involved in human mate selection. The importance of
smell for women. Evol. Hum. Behav. 23, 359 364.
Jacob, S., McClintock, M.K., Zelano, B., Ober, C., 2002. Paternally
inherited HLA alleles are associated with women’s choice of male odor.
Nat. Genet. 30, 175 179.
Klein, J., 1986. Natural History of the Major Histocompatibility Complex.
Wiley, New York.
Koelega, H.S., Kfster, E.P., 1974. Some experiments on sex differences in
odor perception. Ann. N. Y. Acad. Sci. 237, 234246.
Landry, C., Garant, D., Duchesne, P., Bernatchez, L., 2001. Good genes
as heterozygosity: the major histocompatibility complex and mate
choice in Atlantic salmon (Salmo salar). Proc. R. Soc. Lond., B 268,
1279 1285.
Lewis, K., 1998. Pathogen resistance as the origin of kin altruism. J. Theor.
Biol. 193, 359 363.
Manning, C.J., Wakeland, E.K., Potts, W.K., 1992. Communal nesting
patterns in mice implicate MHC genes in kin recognition. Nature 360,
581 583.
Milinski, M., 2003. The function of mate choice in sticklebacks: optimizing
Mhc-genetics. J. Fish Biol. 63 (Suppl. A), 1 16.
Ober, C., Weikamp, L.R., Cox, N., Dytch, H., Kostyu, D., Elias, S., 1997.
HLA and mate choice in humans. Am. J. Hum. Genet. 61, 497 504.
Olse´n, K.H., Grahn, M., Lohmt, J., Langefors, 2., 1998. MHC and kin
discrimination in juvenile Artic charr, Salvelinus alpinus (L.). Anim.
Behav. 56, 319 327.
Olsson, M., Madsen, T., Nordby, J., Wapstra, E., Ujvari, B., Wittsell, H.,
2003. Major histocompatibility complex and mate choice in sand
lizards. Proc. R. Soc. Lond., B Biol. Sci. 270 (Suppl. 2), 254 256.
Pause, B.M., Sojka, B., Krauel, K., Fehm-Wolfsdorf, G., Ferstl, R., 1996.
Olfactory information processing during the course of the menstrual
cycle. Biol. Psychol. 44, 31 54.
Penn, D.J., Potts, W.K., 1998. How do major histocompatibility genes
influence odor and mating preferences? Adv. Immun. 69, 411 435.
Penn, D.J., Potts, W.K., 1999. The evolution of mating preferences and
major histocompatibility complex genes. Am. Nat. 153, 145 164.
Wedekind, C., Fqri, S., 1997. Body odour preferences in men and women:
do they aim for specific MHC combinations or simply heterozygosity?
Proc. R. Soc. Lond., B 264, 1471 1479.
Wedekind, C., Seebeck, T., Bettens, F., Paepke, A.J., 1995. MHC-
dependent mate preferences in humans. Proc. R. Soc. Lond., B Biol.
Sci. 260, 245 249.
Yamazaki, K., Boyse, E.A., Mike, V., Thaler, H.T., Mathieson, B.J., Boyse,
E.A., Zoyas, Z.A., Thomas, L., 1976. Control of mating preferences in
mice by genes in the major histocompatibility complex. J. Exp. Med.
144, 1324 1335.
Yamazaki, K., Yamaguchi, M., Andrews, P.W., Peake, B., Boyse, E.A.,
1978. Mating preferences of F2 segregants of crosses between MHC-
congenic mouse strains. Immunogenetics 6, 253 259.
Ziegler, A., Ehlers, A., Forbes, S., Trowsdale, J., Volz, A., Younger, R.,
Beck, S., 2000. Polymorphisms in olfactory receptor genes: a cau-
tionary note. Hum. Immunol. 61, 1281 1284.
P. Sandro Carvalho Santos et al. / Hormones and Behavior 47 (2005) 384–388388
... Moreover, studies frequently find that men's ratings of women's body odors are not influenced by HLA Santos et al., 2005; but see, . Researchers speculate that women might be more sensitive than men to information about genetic relatedness and immunocompatibility because women invest more heavily in each offspring and, compared to men, their lifetime reproductive potential is lower . ...
... Research demonstrates that humans use HLA-mediated odors to inform mate assessment (for review, Havlicek and Roberts 2009). HLA-disassortative mating may have been selected for in order to increase offspring pathogen resistance by the avoidance of inbreeding Wedekind and Füri 1997;Santos et al. 2005;Roberts et al. 2008). ...
... Whereas earlier studies found that, across vertebrates, including humans, individuals prefer HLA-(i.e., MHC in non-human vertebrates) dissimilar mates (e.g., Santos et al., 2005;; for reviews see, Boyse et al., 1987;, recent meta-analyses reveal this preference is weak in non-human primates and non-significant in humans . If anything, results suggest that humans prefer HLA-diverse (i.e., heterozygous) individuals . ...
Prevalent beliefs in both scientific and popular culture are 1) humans have a poor sense of smell, and 2) smell plays a minimal role in social behavior. However, this consensus is shifting with researchers even suggesting olfaction influences mate choice. Still, studies of odor-based communication in humans remain inconclusive because of poorly designed experiments, scant replication studies, and publication bias. Thus, the goal of this dissertation was to return to first principles and build a solid foundation for the study of human olfaction and mate choice. Chapter 1 provides a rich overview of human olfaction and odor-based communication, revealing the poor methods used in studies of pheromones and body odor. Chapter 2 investigates the impact of a putative female pheromone, copulin, on men’s mating psychology, using rigorous methods (e.g., a placebo-controlled, odor-masking design) and a large sample (n = 243 men). The findings reveal that when the limitations of prior pheromone research are addressed, there is no evidence that copulin is a pheromone. Chapter 3 asks whether some individuals smell more or less attractive to the opposite sex. Studies of mate choice from an evolutionary perspective often begin by investigating whether individuals of one sex agree on the attractiveness level (e.g., facial attractiveness) of individuals of the opposite sex. For comparison, a uniform methodology was used to assess agreement in judgments of physical and vocal attractiveness, modalities in which evidence of shared preferences is generally accepted. No differences were discovered between modalities. Therefore, to the extent shared preferences exist for faces and voices, there is also evidence of shared preferences for body odors. Chapter 4 examines the relationships between independent multisensory judgments of attractiveness (i.e., face, voice, and body odor attractiveness). For men, modalities of attractiveness did not covary. However, in women results indicate weak covariances between all modalities. Moreover, a latent general attractiveness factor (i.e., common fitness correlate) modestly contributed to covariances between modality-specific attractiveness. Together, these findings suggest historical views of human olfaction as unimportant were misguided. In fact, the evidence demonstrates body odor plays a similarly important role to physical and vocal attraction in human mate choice.
... Jacob et al. [18] found that women without using oral contraception preferred body odours of a moderate dissimilar range over body odours of higher or lower similarity. Santos et al. [19] could not reveal an effect of MHC similarity on pleasantness ratings using different olfactory experimental procedures (male versus female, sweat versus urine odour samples). Equally, studies testing men showed no effect of MHC similarity on olfactory ratings [20,21]. ...
... This approach has been used by several authors in several previous studies [21,25,37]. The method, we named 'exact', differentiates between similarity in one or both alleles at a given locus and has been used more frequently [7,16,17,19,[21][22][23]28,29,35]. A high similarity (i.e. in many loci) between partners is considered disadvantageous because it enhances the likelihood for homozygous-and thereby potentially less immuno-competent-offspring. ...
... An advantage of this method is that not only the match between individuals, but also the homozygosity of each individual is considered. Comparison at different typing resolutions: besides determining MHC similarity from the sequencing of the respective genes or exons as for instance performed in [21,25], the MHC similarity can also be determined from the expressed proteins determined in the serum as performed in [7,[16][17][18][19]22,23,30,34,38]. The advantage of the first method is its high precision of typing and the ability to collect samples from saliva instead of blood. ...
Full-text available
Optimization of chances for healthy offspring is thought to be one of the factors driving mate choice and compatibility of the major histocompatibility complex (MHC) is assumed to determine the offspring's fitness. While humans have been claimed to be able to perceive information of MHC compatibility via the olfactory channel, it remains unknown whether humans use such information for mate choice. By investigation of 3691 married couples, we observed that the high polymorphism of MHC leads to a low chance for homozygous offspring. MHC similarity between couples did not differ from chance, we hence observed no MHC effect in married couples. Hormonal contraception at the time of relationship initiation had no significant effect towards enhanced similarity. A low variety of alleles within a postcode area led to a higher likelihood of homozygous offspring. Based on this data, we conclude that there is no pattern of MHC dis-assortative mating in a genetically diverse Western society. We discuss the question of olfactory mate preference, in-group mating bias and the high polymorphism as potential explanations.
... As the number of olfactory neurons declines with age, the elderly have inferior olfactory function to the young, which might affect their body odor sniffing behaviors [10,21]. Besides, body odor plays a significant role in partner choice [23,47] and sexual interest and arousal [15,17,18]. From an evolutionary perspective, young people have greater needs for mate selection and reproduction, and thus may use more body odor cues compared to older people. ...
Objectives Body odor can convey much information about an individual and thus we frequently engage in sniffing one's own and other people's body odor. However, there is scarce evidence on the within- and cross-cultural variation in body odor sniffing behaviors and no psychometric scale for specifically measuring such behaviors. Hence, our study aimed to develop the Body Odor Sniffing Questionnaire (BOSQ) and used it to make a cross-cultural comparison. Methods In Study 1, 2,026 participants were recruited from our university, with one half used for exploratory factor analysis (EFA) to examine the factor structure of the BOSQ (sample 1) and the other half used for confirmatory factor analysis (CFA) to verify the factor structure (sample 2). In Study 2, 352 Chinese and 254 US participants were recruited to complete the BOSQ through Wenjuanxing and Amazon Mechanical Turk, enabling comparison of body odor sniffing behaviors across two cultures. Results The Study 1 results showed that the BOSQ comprises 17 items in three factors: self-private body odor, others’ body odor, and self-common body odor. The CFA results further supported that this three-factor model was a good fit. The Study 2 results showed that US participants scored higher overall and on the self-private body odor and others’ body odor dimensions, whereas Chinese participants scored higher on the self-common body odor dimension. Conclusions The BOSQ demonstrated good reliability and validity, which is a useful tool for evaluating individuals’ body odor sniffing behaviors. Cross-cultural difference existed as the US population reported a higher prevalence of body odor sniffing behavior, compared to the Chinese population.
... Single women who were not in a relationship preferred MHC similar men, while those in a relationship preferred MHC dissimilar men. The results regarding women's odor preferences for MHC similar men while on hormonal contraceptives had been found in three previous studies (Wedekind et al., 1995;Wedekind and Furi, 1997;Santos et al., 2005), while two other studies showed an intermediate (Jacob et al., 2002) and a null effect (Thornhill, 2003). ...
Full-text available
In the past decade, two large prospective cohort studies of British and American women have been conducted which found a statistically significant increase in the risk of violent death in ever-users of hormonal contraceptives. Research on the effects of hormonal contraceptives upon the behaviors of intimate partners and on the physiology of women using hormonal contraceptives has provided insight into the possible basis for the resulting increase in violent death. This review examines the changes that are potential contributors to the reported increase.
... There is also a literature on MHC, a set of genes involved in immune function. This olfactory signature provides clues as to the genetic compatibility (i.e., viability/health) of any potential offspring (Chaix et al., 2008;Havlicek & Roberts, 2009;Penn et al., 2002;Roberts et al., 2005aRoberts et al., , 2005bSantos et al., 2005;Wedekind et al., 1995;Winternitz et al., 2017; see also Jacob et al., 2002). Perhaps unsurprisingly, the growing evidence concerning the informative nature of a person's body odour in terms of chemosensory communication (Russell, 1976) has also led to growing artistic interest in the idea of the smell dating agency The basic idea here is that people choose their date based on the unfragranced smell of t-shirts after having been worn (Jamieson, 2016). ...
Full-text available
In recent decades, there has been an explosion of research into the crossmodal influence of olfactory cues on multisensory person perception. Numerous peer-reviewed studies have documented that a variety of olfactory stimuli, from ambient malodours through to fine fragrances, and even a range of chemosensory body odours can influence everything from a perceiver’s judgments of another person’s attractiveness, age, affect, health/disease status, and even elements of their personality. The crossmodal and multisensory contributions to such effects are reviewed and the limitations/peculiarities of the research that have been published to date are highlighted. At the same time, however, it is important to note that the presence of scent (and/or the absence of malodour) can also influence people’s (i.e., a perceiver’s) self-confidence which may, in turn, affect how attractive they appear to others. Several potential cognitive mechanisms have been put forward to try and explain such crossmodal/multisensory influences, and some of the neural substrates underpinning these effects have now been characterized. At the end of this narrative review, a number of the potential (and actual) applications for, and implications of, such crossmodal/multisensory phenomena involving olfaction are outlined briefly.
... Conclusión: el olor y el HLA intervienen en la elección de la pareja. No faltan confirmaciones parciales o totales, con y sin camisetas 5,6 . Sin embargo, en un recién publicado meta-análisis, a 25 años de la primera publicación de Wedekind, que incluye las publicaciones propias de los analistas, estos mismos admiten "humildemente" que nuestro conocimiento es incompleto y que, "tristemente", no pueden concluir que las preferencias asociadas al MHC afecten en la vida real la elección de la pareja y, si lo hacen, en cuales circunstancias 7 . ...
Human love signals are nonverbal signs of sexual attraction, courtship, seduction, and love. Myriad signs, signals, and cues of attraction are in service to what the authors call the “reproductive force,” the fifth fundamental force of nature after the strong, weak, electromagnetic, and gravitational forces of physics. The reproductive force appeared some 3.7 billion years ago with RNA and later, DNA, in the origin of life on Earth. RNA and DNA molecules encode information (via codons) about how to reproduce themselves. Selfishly enforced, guided, and shaped by primordial messaging molecules, self-replication became the prime directive—the summum bonum or “greatest good”—of life and living, pursued for its own sake and solely on its own behalf. The reproductive force remains a potent motivator in humans today, in their overall demeanor, facial expressions, gestures, goals, clothing, automobiles, music, media, art, religion, hairdos, shoes, prom dresses, and diverse additional nonverbal signs and cues. This chapter explores the relationship between love signals and the overarching reproductive force.
Full-text available
Inbreeding and low diversity in MHC genes are considered to have a negative effect on reproductive success in animals. This study presents an analysis of the number and body mass of offspring in domestic cat, depending on the inbreeding coefficient and the degree of similarity in MHC genes of class I and II in parents. Inbred partners had a lower number of live kittens at birth than outbred ones. At the same time, the inbreeding coefficient did not affect the litter size and the number of offspring who survived until the period of transition to solid food. The most significant predictor for the number of surviving offspring was the degree of parental similarity in MHC genes: the parents with the maximum distance in MHC genes had more survived kittens. Moreover, this effect was most pronounced immediately after birth. A significant percentage of kittens from parents with a minimum distance in MHC genes were either stillborn or died on the first day after birth. By the age of transition to solid food, this effect is no longer so pronounced. Furthermore, neither the inbreeding coefficient nor the distance in MHC genes of parents had any effect on the body mass of kittens.
In many species, social communication and mate choice are influenced by olfactory cues associated with the major histocompatibility complex (MHC). It has been reported that humans also respond to olfactory signals related to the human MHC-equivalent, the Human Leucocyte Antigen (HLA)-System, and exhibit an olfactory-mediated preference for potential mating partners with a dissimilar, disassortative, HLA-type compared to their own. The aim of this study was to investigate whether HLA-associated peptides, presented as volatile cues, elicit neuronal responses at the receptors in the human olfactory epithelium and can be consciously perceived. To this end the discrimination ability for peptides was tested in a 3-alternative forced choice model. Furthermore electro-olfactograms of the olfactory epithelium and EEG-derived chemosensory event related potentials were recorded using precisely controlled olfactometric stimulation with peptides and control odors. Based on responses from 52 young, healthy participants the peptides could not be discriminated and the electrophysiological signals provided no evidence for a specific response to the peptides which was in contrast to the control odors. In conclusion, within the current setup the results suggest that HLA-associated peptides do not produce specific olfactory activation in humans.
Sexual imprinting refers to the phenomena where an individual's mate selection behavior is influenced by the characteristics of their parents in the early stages of life. Previous studies revealed that heterosexual men and women prefer partners with personality traits similar to their opposite-sex parents, indicating the sexual imprinting effects in personality preferences. This study aims to examine whether there are sexual imprinting effects on partner preferences for personality traits in gay men. We tested whether parent-child relationship in childhood (before 12 years old) and/or adolescence (12–18 years old) moderated the sexual imprinting effects. Participants (N = 311) were asked to assess their parents' and ideal partner's Big Five personality traits and gender roles, respectively. The parent-child relationships in childhood and adolescence were also assessed. The results revealed that gay men's ideal partner's traits were similar to their fathers' traits for emotional stability, similar to their mothers' traits for agreeableness and openness, and similar to both their fathers' and mothers' traits for conscientiousness. The ideal partners' gender roles were similar to both mothers' and fathers' instrumentality and expressiveness. The relationship quality with the mother in childhood modulated the mating effects in conscientiousness and expressiveness. The relationship quality with the father in adolescence modulated the mating effects in masculine instrumentality. The findings indicated the sexual imprinting effects on partner preference for personality traits in gay men and both father's and mother's personality traits in shaping gay's partner preference.
Full-text available
A survey study examining the relative importance of various social and physical traits in heterosexual attraction was conducted. Data from 198 male and female heterosexual college students revealed that women ranked body odor as more important for attraction than “looks” or any social factor except “pleasantness.” Moreover, in contrast to response to fragrance use, liking someone's natural body odor was the most influential olfactory variable for sexual interest for both men and women. Men rated a woman's good looks as most desirable and as more important than any other factor except pleasantness. Sex differences in the relative ranking of several social factors were consistent with prior research.
Full-text available
This study examined the relationship between the major histocompatibility complex (MHG) genes and mate choice by wild house mice in a controlled laboratory setting in an attempt to understand the mechanisms maintaining natural MHC diversity. Three rearing groups of wild test mice were produced: nonfostered control mice, mice fostered into families of an inbred laboratory mouse strain, and mice fostered into families of a second mouse strain differing genetically from the first only within the MHC region. At maturity test mice were given a choice of two opposite-sex stimulus mice of the two MHC-congenic strains used for fostering. Test mice were scored for several measures of preference including amount of time spent with either stimulus mouse, and ejaculation with a stimulus mouse. Females in mio of three rearing groups spent more time with one MHC type regardless of rearing environment, suggesting that females did not prefer mates dissimilar from family MHC type. Time preferences tended to he: stronger in females than in males. Male test mice ejaculated indiscriminately. Female wild mice mated to ejaculation more often in longer trials, but these matings were still too infrequent to assess preferences. Fostering had little or no effect on MHC-based mate preferences of wild house mice, and no evidence suggested that MHC was used to avoid inbreeding. Wild female mice may still choose mates based on MHC haplotypes (but do not necessarily prefer MHC-dissimilar mates); other cues are probably also used. Based on these results, inbreeding avoidance does not seem a strong mechanism for maintaining natural MHC diversity.
What roles do mesolimbic and neostriatal dopamine systems play in reward? Do they mediate the hedonic impact of rewarding stimuli? Do they mediate hedonic reward learning and associative prediction? Our review of the literature, together with results of a new study of residual reward capacity after dopamine depletion, indicates the answer to both questions is 'no'. Rather, dopamine systems may mediate the incentive salience of rewards, modulating their motivational value in a manner separable from hedonia and reward learning. In a study of the consequences of dopamine loss, rats were depleted of dopamine in the nucleus accumbens and neostriatum by up to 99% using 6-hydroxydopamine. In a series of experiments, we applied the 'taste reactivity' measure of affective reactions (gapes, etc.) to assess the capacity of dopamine-depleted rats for: 1) normal affect (hedonic and aversive reactions), 2) modulation of hedonic affect by associative learning (taste aversion conditioning), and 3) hedonic enhancement of affect by non-dopaminergic pharmacological manipulation of palatability (benzodiazepine administration). We found normal hedonic reaction patterns to sucrose vs. quinine, normal learning of new hedonic stimulus values (a change in palatability based on predictive relations), and normal pharmacological hedonic enhancement of palatability. We discuss these results in the context of hypotheses and data concerning the role of dopamine in reward. We review neurochemical, electrophysiological, and other behavioral evidence. We conclude that dopamine systems are not needed either to mediate the hedonic pleasure of reinforcers or to mediate predictive associations involved in hedonic reward learning. We conclude instead that dopamine may be more important to incentive salience attributions to the neural representations of reward-related stimuli. Incentive salience, we suggest, is a distinct component of motivation and reward. In other words, dopamine systems are necessary for 'wanting' incentives, but not for 'liking' them or for learning new 'likes' and 'dislikes'.
Publisher Summary This chapter discusses the information contained in the odorous secretions of mammals and provides a classification system based on the behavioral and chemical analyses. This classification divides social odors into two groups: identifier and emotive. Identifier odors are defined as those produced through the regular metabolic processes of the animal, without specific stimulation. The emotive odors are those produced as the result of some transient emotional state or external stimulus. The chapter categorizes nine different types of information contained in mammalian social odors: species, age, sex, colony membership, individuality, social status, reproductive state, maternal state, and stress odors. Social odors are modified by diet and hormone levels and by bacterial action. When the chemicals and bacteria responsible for producing the social odors have been identified, the responses of test animals show large individual differences. Responses to olfactory stimuli depend on hormonal and experiential factors. Theoretical models in the study of population regulation, sexual selection, kinship recognition, altruism, parental care, and territoriality infer that animals recognize particular individuals and specific relationships, and such recognition may depend to some extent on the information contained in olfactory signals.
When a male mouse is presented with two H-2 congenic two female in estrus, his choice of a mate is influenced by their H-2 types. The term "strain preference" is used to describe the general tendency of the male population of one inbred strain to prefer two female of one H-2 type rather than another. The term "consistency of choice" is used to describe the added tendency of particular two males of one inbred strain, in sequential mating trials, to prefer two females of the H-2 type they chose in previous trials. Statistical analysis showed trends in the data that support the following conclusions: (a) The choice is made by the male, not the female. (b) The strain preference of two males may favor two females of dissimilar H-2 type (four of six comparisons), or of similar H-2 type (one of six comparisons). (c) Consistency of choice does not always correspond with strain preference. In one of six comparisons of H-2 genotypes there was no strain preference but pronounced consistency of choice by individual two male.This suggests memory, but fortuitous bias is not excluded. (d) Strain preference of the same male population may favor two male of the same or a different H-2 type, depending on which different H-2 type is offered as the choice alternative to self.These findings conform to a provisional model in which olfactory mating preference is governed by two linked genes in the region of H-2, one for the female signal and one for the male receptor. These mating preferences could in natural populations serve the purpose of increasing the representation of particular H-2 haplotypes or of maintaining heterozygosity of genes in the region of H-2.
Sexual reproduction is an evolutionary ‘puzzle’. A sexual female ‘throws away’ half of her genes (during meiosis), and ‘fills up’ what she lost with genes from a male. Thus, sexual reproduction can only be successful if the offspring with the new mixture of genes should be more than twice as fit as if she had just made a copy of herself. A challenging hypothesis assumes that infectious diseases select for females that reshuffle the immune genes for their offspring in each generation. The required increase in quality could be achieved by females selectively ‘smelling out’ suitable immune-genes (i.e. Mhc alleles) in potential partners, which, in combination with the female's genes, offer optimal resistance against quickly changing infectious diseases. It was found that most three spined sticklebacks Gasterosteus aculeatus in natural populations around Plön, Germany, had intermediate instead of maximal numbers of different Mhc class IIB alleles. Furthermore, fish with an intermediate number of different Mhc alleles were infected with the lowest number of both parasite species and parasites per species. This suggests that Mhc heterozygosity was optimized instead of maximized. Can this immunogenetic optimum be achieved through female choice? In a flow channel design that allowed the detection of olfactory signals only, it was found that female three-spined sticklebacks that were ready to spawn preferred males as mates that in combination with their Mhc alleles would allow the production of offspring with the optimal number of Mhc alleles. Thus, mate choice in three-spined sticklebacks could have the two-fold advantage over asexual reproduction that is required to maintain sexual reproduction. The interaction of olfactory with visual signals in three-spined stickleback mate choice is discussed. The three-spined stickleback is a suitable model organism for studying the evolution of sexual reproduction in relation to optimizing offspring immune genetics although other fishes may be as suitable.
Male and female F2 homozygotes from crosses between MHC-congenic inbred mouse strains were tested for MHC-associated mating preference. In three instances, of the four genotypic combinations so tested, marked MHC-associated mating preference was observed. This result greatly reduces the possibility that the observed mating preferences of MHC-congenic inbred strains can be explained wholly in terms of non-MHC genetic drift, or of residual non-MHC genetic disparity, or of fortuitous acquired strain characteristics unrelated to MHC. In two of the four combinations investigated, the MHC-related mating bias of F2 segregants was similar to that of the genotypically similar inbred parent strains. In a third combination, F2 segregants did not show the mating bias exhibited by the corresponding parent strains. In a fourth combination, F2 segregants displayed an MHC-related mating bias that was evident in the corresponding parental inbred strains only when the colonies of the parent strains had been maintained in isolation from other strains. While the exhibition of mating preference by mice of the same genotypes may differ according to circumstances, as indicated, in no instance was preference reversed. Mating preference in a given combination of MHC genotypes, whenever it was observed, always favored the same MHC haplotype of the two alternative haplotypes represented. It appears that the familial MHC genotypes of mice and the environment in which the colonies are maintained influence their MHC-related mating preference, but it has yet to be decided whether these factors operate by determining exposure to particular MHC haplotypes.