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Paternally inherited HLA alleles are associated with women's choice of male odor

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Abstract

The major histocompatibility complex (MHC) is a source of unique individual odors that influence individual recognition, mating preferences, nesting behavior and selective block of pregnancy in animals. Such phenomena have been difficult to study in humans, because the human leukocyte antigen (HLA, human MHC) loci are the most polymorphic loci in the human genome, with the potential to generate millions of unique combinations of genotypes. In addition, high variability in background odors, encoded by the rest of the genome and influenced by cultural practices, contribute to a low signal-to-noise ratio that could mask HLA-based olfactory cues. Here we show that women can detect differences of one HLA allele among male odor donors with different MHC genotypes. Notably, the mechanism for a woman's ability to discriminate and choose odors is based on HLA alleles inherited from her father but not her mother. The parents' HLA alleles that she does not inherit show no relationship with odor choice, despite exposure to these HLA-encoded odors throughout her life. Our data indicate that paternally inherited HLA-associated odors influence odor preference and may serve as social cues.
article
nature genetics •
volume 30 • february 2002
175
Paternally inherited HLA alleles are
associated with women’s choice
of male odor
Suma Jacob1, Martha K. McClintock1*, Bethanne Zelano1& Carole Ober2*
*These authors contributed equally to this work.
Published online: 22 January 2002, DOI: 10.1038/ng830
The major histocompatibility complex (MHC) is a source of unique individual odors that influence individual
recognition, mating preferences, nesting behavior and selective block of pregnancy in animals1–10. Such phenom-
ena have been difficult to study in humans, because the human leukocyte antigen (HLA, human MHC) loci are the
most polymorphic loci in the human genome11, with the potential to generate millions of unique combinations of
genotypes. In addition, high variability in background odors, encoded by the rest of the genome and influenced
by cultural practices, contribute to a low signal-to-noise ratio that could mask HLA-based olfactory cues. Here we
show that women can detect differences of one HLA allele among male odor donors with different MHC geno-
types. Notably, the mechanism for a woman’s ability to discriminate and choose odors is based on HLA alleles
inherited from her father but not her mother. The parents’ HLA alleles that she does not inherit show no relation-
ship with odor choice, despite exposure to these HLA-encoded odors throughout her life. Our data indicate that
paternally inherited HLA-associated odors influence odor preference and may serve as social cues.
1Institute for Mind and Biology and Department of Psychology, 5730 South Woodlawn Avenue, The University of Chicago, Chicago, Illinois 60637, USA.
2Department of Human Genetics, University of Chicago, Chicago, Illinois, USA. Correspondence should be addressed to M.K.M. (e-mail:
mkm1@midway.uchicago.edu).
Introduction
It is often assumed incorrectly that humans have a poorly devel-
oped sense of olfactory perception12,13. In fact, there are some
molecules to which humans are extremely sensitive (the thresh-
old for detecting 2-bromophenol is 10–4.6 ppm)14. People can
also detect the odors encoded by genetic information, discrimi-
nating between nearly identical strains of mice that differ only at
one or a few MHC loci15. In addition, individuals have described
body odors to be pleasant when they are from people who have
few HLA alleles that match their own16,17.
We sought to determine the resolution of the human ability to
discriminate among HLA-associated odors by investigating
women’s odor choice based on the number of matches to their
own HLA. Because odor choice could be based solely on expo-
sure to MHC-associated odors from one’s family during develop-
ment18–20 or could require information from one’s inherited
HLA, we carried out a human odor choice study in an isolated
community for which the HLA types of two generations are
known21. For the first time, we were able to determine whether a
woman’s choice of HLA-associated odors were based on alleles
inherited from her father, mother or both, or on exposure to
nontransmitted parental HLA alleles. In addition, in contrast to
the virtually unlimited number of HLA haplotypes present in
outbred populations, there are only 67 HLA haplotypes in this
community22. Forty-nine unmarried women who had never
been pregnant participated in the olfactory choice sessions.
We selected as odor donors men of diverse ethnicity and a
different ethnicity compared with that of the isolated commu-
nity, but who nonetheless carried HLA alleles found in the
community as well as completely foreign alleles (Fig. 1). At each
of the five HLA loci studied, there was a possibility of up to two
allele matches, for a maximum of ten matches. Our sample con-
tained a median of two allele matches (range 0–7) between the
smellers and the odor donors. To collect body odors, each
donor wore the same T-shirt for two consecutive nights. The
women were not told the source of the odors. They rated each
T-shirt odor for four attributes: familiarity, intensity, pleasant-
ness and spiciness. Unexpectedly, the women in our study rated
the human odors in absolute terms as slightly pleasant and
more pleasant than common household odors (Table 1).
Results
Odor choices and HLA matches
To determine whether women prefer odors on the basis of an
individual’s HLA type, we asked the women which odor they
would choose and which they would not choose, if they had to
smell it all the time. There were no differences among donors in
their likelihood of being chosen either as the most or the least
preferred by the women as a group (χ2=2.3, df=5, P=0.81).
There were significant differences only relative to each
womanthat is, the combination of a particular woman and
odor donor. The donor of a woman’s most preferred odor had
© 2002 Nature Publishing Group http://genetics.nature.com
article
176 nature genetics •
volume 30 • february 2002
significantly more HLA allele matches with her own alleles than
did the donor of her least preferred odor (Fig. 1; Wilcoxon
paired sign test, P=0.0016). Specifically, a woman’s most pre-
ferred odors were from donors who had 2.3 ±0.2 matches with
her own HLA alleles, significantly more matches than with
donors of her least preferred odors (1.5 ±0.2; paired t-test:
t=3.65, P=0.0007). Thus, women can discriminate between
odors from donors with different HLA types whose number of
HLA matches differed on average by only one allele. Notably,
this discrimination took place even though women were tested
without regard to menstrual cycle phase, which modulates
olfactory perception23.
123456loci 123456loci
11, 31 2, 24 2, 2 2, 2 2, 25 11, 29 HLA-A 11, 31 2, 24 2, 2 2, 2 2, 25 11, 29 HLA-A
2, 4 5, 7 3, 5 4, 5 7, X 4, 7 HLA-C 2, 4 5, 7 3, 58 4, 5 7, X 4, 7 HLA-C
27, 35 7, 44 8, 58 18, 35 7, 18 7, 35 HLA-B 27, 35 7, 44 8, 5 18, 35 7, 18 7, 35 HLA-B
1, 4 4, 13 3, 13 3, 12 15, 15 4, 7 HLA-DR 1, 4 4, 13 3, 13 3, 12 15, 15 4, 7 HLA-DR
302, 501 302, 303 201, 603 301, 201 602, 602 302, 201 HLA-DQB1 302, 501 302, 303 201, 603 301, 201 602, 602 302, 201 HLA-DQB1
1
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
2
51
4
301
24
3
60
15
602 2322
3M1L26
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
4
35
1
501
2
3
60
4
402 522
3L1M3
2
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
2
51
4
301
24
7
8
3
201 24M4L423 27
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
X
51
4
301
2
3
62
4
302 3422
1M3L
3
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
2
51
4
301
1
6
57
7
303 23M121
2L28
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
X
51
4
301
2
3
62
4
302 3422
1L3M
4
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
1
2
27
11
301
1
6
57
7
303 2M1010
1L29
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
X
51
10
501
26
X
38
15
602 1100
2M0L
5
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
2
27
1
501
24
4
35
16
502 610
2L02M30
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
1
7
8
3
201
26
X
38
15
602 01M323
2L
6
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
32
3
62
4
302
32
X
35
11
301 321
2L03M31
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
X
51
4
301
1
6
57
7
303 1L2010
2M
7
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
32
3
62
4
302
32
X
35
11
301 321
2L03M32
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
7
8
3
201
2
6
50
3
201 0L3M6523
8
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
X
51
13
603
2
2
51
4
301 24M43
2L133
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
1
6
57
7
303
2
3
62
4
302 242
1M1L3
9
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
1
7
8
3
201
26
X
38
15
602 01L323
2M34
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
2
51
4
301
1
6
57
7
303 231L21
2M
10
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
2
27
1
501
1
6
57
7
303 4M100
0L135
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
3
62
4
302
1
2
27
11
301 4L3221
2M
11
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
2
27
1
501
2
1
27
8
402 511
1M10L36
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
11
4
35
1
501
2
2
51
4
301 721
4L14M
12
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
X
51
4
301
1
6
57
7
303 1M201
0L237
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
X
51
10
501
26
X
38
15
602 1L1M0020
13
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
7
8
3
201
2
3
62
4
302 2L5532
4M38
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
X
51
10
501
2
3
60
15
602 12L2M130
14
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
3
62
4
302
3
X
51
4
301 342
2L1M339
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
2
51
4
301
24
X
51
10
501 3M31L211
15
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
3
62
4
302
3
2
27
1
501 6321
1L2M40
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
4
35
16
502
1
2
27
11
301 4103
0L2M
16
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
7
8
3
201
1
7
8
3
201 03M642
4L41
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
4
35
16
502
24
3
60
15
602 2212
2L2M
17
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
7
8
3
201
2
3
62
4
302 2L55M324 42
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
26
X
38
15
602
26
X
38
15
602 00M0L040
18
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
X
51
13
603
1
6
57
7
303 033
1M11L43
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
X
51
13
603
24
5
44
1
501 254
2M10L
19
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
32
X
35
11
301
1
6
57
7
303 1102
0L2M44
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
X
51
13
603
2
3
62
4
302 255
2L2M2
20
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
32
X
35
11
301
11
4
35
1
501 600M40L445
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
6
57
7
303
2
3
62
4
302 2M5L2113
21
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
1
7
8
3
201
2
3
60
4
402 1L35M323 46
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
4
35
1
501
2
3
60
4
402 52L231
3M
22
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
24
X
51
3
201
26
1
56
4
201 123M30
3L47
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
4
35
1
501
1
2
27
11
301 60L03
0M2
23
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
2
X
51
13
603
31
7
7
4
301 2L532
3M348
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
2
27
1
501
2
1
27
8
402 5M11L110
24
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
X
51
4
301
1
6
57
7
303 120L10
2M49
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
1
2
27
11
301
1
6
57
7
303 21L01M01
25
HLA-A
HLA-C
HLA-B
HLA-DR
HLA-DQB1
3
4
35
1
501
24
3
60
15
602 41L121
2Mmean ± SEM,
min-max allele
matches
2.5 ± 0.27,
0–7 2.4 ± 0.21,
0–5 1.9 ± 0.25,
0–6 2.0 ± 0.16,
0–5 1.22 ± 0.15,
04 2.1 ± 0.17,
0–4
smellers
donors
paternal haplotype
maternal haplotype
smellers
donors
paternal haplotype
maternal haplotype
Fig. 1 Number of allele matches between each smeller/donor pair. The genotypes at the five HLA loci of each of the six donors are shown in the top six rows. The
HLA alleles on the paternally inherited and maternally inherited haplotypes are shown for each of the 49 smellers in the first six columns. The final row gives the
mean, standard error of the mean and range of allele matches with all 49 women for each odor donor. The superscript M indicates the most preferred donor
odor, and the superscript L indicates the least preferred, for each woman. The following donor alleles were not present in the study population: B58 (donor 3),
DR12 (donor 4), A25 (donor 5), and A29 (donor 6).
© 2002 Nature Publishing Group http://genetics.nature.com
Odor characteristics and identification
Before making their odor choices, women had rated their most pre-
ferred odors as more pleasant (mean 1.2 ± 0.41 versus –0.7 ± 0.42;
paired t-test: t
(48df)
=3.77, P=0.0004) and less spicy (mean –1.3
± 0.47 versus 0.1 ± 0.50; paired t-test: t
(48df)
=–2.62, P=0.01)
than their least preferred odors, but did not rate them as more
familiar (mean 5.4 ± 44 versus 5.2 ± 0.45; paired t-test:
t
(48df)
=0.27, P=0.79) or intense (mean 5.8 ± 0.40 versus 6.1 ± 0.35;
paired t-test: t
(48df)=
–0.87, P=0.39). Although the most preferred
odors were from donors with more HLA matches than the least
preferred, they were not perceived as being more familiar. More-
over, the women were unaware of the source of the odors, and only
19% of the women described the donor odors as possibly being
related to anything associated with humans (such as a closet).
Most of the women, therefore, made these judgments without
being conscious of them as natural human odors.
Paternally versus maternally inherited HLA
We next asked whether these HLA-associated odor choices were
related to the parental origin of the matched alleles. We exam-
ined separately the number of matches between each donor and
the HLA alleles that the woman inherited from her mother ver-
sus those that she inherited from her father. The results indicate
that a woman’s choices were based on matches to the alleles
inherited from her father (1.39 ± 0.15 matches with most pre-
ferred donor versus 0.55 ± 0.10 matches with least preferred
donor, paired t-test, t(48df)=4.57, P<0.0001), but not on matches
to the alleles inherited from her mother (0.90 ± 0.11 matches
with most preferred donor versus 0.94 ± 0.13 matches with least
preferred donor, paired t-test, t(48df)=–0.31, P=0.76).
To determine whether there was a linear dose-dependent relation-
ship between increasing number of allele matches and strength of
preference, we examined the number of paternally inherited
matches for each woman and the
preference rank she assigned to
each odor donor. We found that
the more matches to the pater-
nally inherited alleles there were,
the higher the donor’s rank, in
contrast to the maternally inher-
ited alleles, for which there was
no such relationship (Fig. 2). In
addition, the regression between
the number of matching inher-
ited alleles and preference rank was significantly different for the
paternal and maternal alleles (heavy red lines in Fig. 2).
Developmental mechanisms
Finally, we sought to determine whether the observed HLA odor
choices required the inheritance of paternal alleles or could be
explained by exposure to both the inherited and noninherited
paternal HLA alleles during development. Because the HLA type
of each parent was known, we were able to ask whether a woman
had to inherit her father’s HLA alleles that matched those of the
donor to manifest a preference, or whether postnatal exposure to
her father’s HLA was sufficient. In the latter case, there would
also be a correlation between the HLA alleles of preferred donors
and those present in her father that she did not inherit. A
woman’s preference was associated only with matches to inher-
ited paternal alleles and not to the paternal alleles that she did not
inherit (three-factor repeated measures ANOVA, Fig. 3). More-
over, she did not base odor choices on matches with her mother’s
HLA alleles that she did not inherit (Fig. 3). Thus, women’s odor
choice is associated with inherited HLA alleles and not just on
postnatal exposure to the parents’ HLA, although environmental
exposures could affect patterning choices.
Discussion
This is the first study in humans, or in any species, to demonstrate
that HLA-associated odor choices are determined by paternally
inherited HLA alleles and that exposure to the HLA-associated
odors of one’s family is not sufficient for determining preference.
Our results indicate that women have an exquisitely sensitive olfac-
tory system that allows them to make choices based on small differ-
ences in HLA alleles: preferred odor donors had an average of 1.4
allele matches, and the least preferred donors had an average of 0.6
allele matches to a woman’s paternally inherited haplotype (Fig. 3).
Fig. 2 Number of matching HLA alleles
and odor choice. Individual regres-
sions between the number of donor
alleles matching a woman’s alleles and
her preference rank of the six donors
(a rank of 6 was the most preferred).
a, This analysis includes only the 22
women who had at least three differ-
ent paternal matching scores (individ-
ual ranges between 0–2 and 0–5
matching alleles) among the six
donors. Average slope coeffi-
cient=0.62 ± 0.15, t=4.0, P=0.001; aver-
age intercept=2.7 ± 0.2, t=–4.8,
P=0.001. b, Individual regressions for
the 18 women whose matches
between maternal and donor alleles
met the same range criteria as in a.
Average slope coefficient=–0.27 ± 0.19,
t=–1.34, P=0.19; average intercept=3.8
± 0.2, t=1.3, P=0.20. Heavy red lines in a
and brepresent the ten women who
met the above criteria for both their
paternally inherited and maternally inherited alleles and thus contributed to both panels in the figure. Their paternal and maternal regressions were significantly
different (slope coefficients: 0.70 ± 0.08 versus –0.38 ± 0.23, paired t=4.2, P=0.002; intercepts: 2.6 ± 0.01 versus 3.8 ± 0.2, paired t=4.9, P=0.001).
article
nature genetics •
volume 30 • february 2002
177
Table 1 • Average ratings for attributes of each type of odor (paired t-test comparisons
within subjects of men’s odor versus bleach, clove and control)
Odor
Attribute Scale Men Bleach Clove Control
Familiarity 0 to 10 5.5 ± 0.29 9.6 ± 0.14a7.3 ± 0.44b6.2 ± 0.35c
Intensity 0 to 10 5.1 ± 0.22 9.1 ± 0.21a9.1 ± 0.20a4.4 ± 0.28d
Pleasantness –5 to 5 0.2 ± 0.27 –0.08 ± 0.50 –0.90 ± 0.48c1.1 ± 0.25d
Spiciness –5 to 5 –1.2 ± 0.28 1.6 ± 0.53a4.5 ± 0.20a–2.6 ± 0.29a
Difference from men’s odor: aP0.0001; bP0.001; cP0.05; dP0.01.
6
5
4
3
2
1012345
6
5
4
3
2
1012345
number of matches
number of matches
rank of donor
rank of donor
paternally inherited alleles maternally inherited alleles
ab
© 2002 Nature Publishing Group http://genetics.nature.com
article
178 nature genetics •
volume 30 • february 2002
No other studies have revealed a preference for a small number of
MHC allele matches over fewer matches (that is, one or none). This
is not inconsistent, however, with the results of previous studies in
which the choices offered were between individuals with a small
number of allele matches and those with identical or nearly identi-
cal MHC. Studies of inbred mouse strains4,7,9 and humans21,24
have revealed avoidance of mates with a very high number of
matching alleles (with one or two haplotypes identical to one’s
own). When given a choice of self or different MHC, there is a con-
sistent preference for differences. Our study investigated choices
within the lower range of 0–7 allele matches; the results show that
women avoid odors from donors with 0 or 1 HLA allele matches to
their own HLA alleles and prefer odors from donors with more
HLA matches. Our study is thus consistent with previous literature,
showing that a small, intermediate number of MHC matches is
preferred over either zero matches or identical MHC.
This finding is different from the results of two studies by
Wedekind and colleagues16,17, who reported that female students
tended to describe body odors as pleasant when from someone with
few HLA allele matches to their own HLA (r=–0.15, one-tailed
P=0.07)17. Although these studies examined HLA matching in the
same range as in our study, they did not use an odor preference
choice test (‘wanting’)25, which has a different neural substrate than
judgments of pleasantness (‘liking’)25. Moreover, they did not evalu-
ate the individual effects of the maternally inherited and paternally
inherited alleles on odor perception. Additional differences in study
design, such as selecting donors and recipients from the same popu-
lation, make it difficult to directly compare Wedekind and colleagues’
study16,17 with the results of this study or the existing literature.
Why would an intermediate number of MHC matches be opti-
mal? It has been shown that female mice prefer males that are just
slightly unfamiliar over those that are either very familiar or very
unfamiliar26. This preference might result in an optimal balance
between inbreeding and outbreeding costs27,28. More recently, it
was hypothesized29 that a preference for mates with intermediate
levels of MHC matching may be an optimal evolutionary strategy
to preserve immunocompetence of offspring. Our data are con-
sistent with these proposals and suggest that when people are
presented with choices among individuals with levels of MHC
disparity that would typically be encountered in outbred, natural
populations, they have a preference for more matches.
The evolutionary significance of MHC-based odor preferences
has been narrowly interpreted as a potential mechanism for mate
choice; however, MHC-based odor choices may influence broader
aspects of social behavior, such as communal nesting10 and other
forms of kin-biased behavior. For example, adult female baboons
(Papio cynocephalus) groom and aid their paternal half-sisters
more than non-kin, biasing their social behavior as much or even
more than they do toward maternal half-sisters30. This ability to
recognize paternal kin is notable because in this promiscuous
species, paternity is unknown and adult males do not participate
in childrearing. Olfactory recognition of paternally inherited
MHC could help a female to recognize paternal kin in this and
other species where paternity is not certain.
The main olfactory system has the potential to decode MHC
information31. The multiple receptors and neural pathways of the
olfactory system distinguish small differences in a large repertoire
of molecular structures32 and thus could mediate the discrimina-
tion between gene products of one HLA allele, as seen in this study.
In humans and mice, and perhaps other animal species as well, the
detection of MHC-mediated body odor may result from the close
linkage between the MHC loci and olfactory receptor genes33,34.
MHC-specific odors may be soluble MHC proteins or their vagile
components, odor molecules bound selectively to MHC proteins,
or by-products of MHC-specific bacteria colonization in skin or
axillae35–37. Moreover, an inherited parent-of-origin effect on odor
preferences has been reported in mice38, albeit for general body
odor and not specifically for MHC-derived odors, showing that
olfactory systems can distinguish between paternally and mater-
nally inherited genetic information.
This is the first double-blind study of MHC-derived odor choices
in humans, and the first to reveal a paternally inherited component
associated with these choices. We have shown that a woman’s odor
choice is associated with inherited HLA alleles rather than exposure
to HLA-associated odors from her family during development.
Consistent with earlier studies, these data indicate that there is not
one most preferred human male odor for everyone, but that odor
preference is relative, based in this case on the degree of HLA differ-
ences between a man and a woman.
Methods
Sample composition. Members of the community are of German-Austrian
descent. Unmarried women (n=49; average age 25 ±1.6 y ; range=13 y to 56 y)
participated in olfactory sessions. They were all raised by their biological par-
ents and all but one were members of large families (median sibship size=7;
range 4–11). All were at least one year past menarche and all but one (age 56)
had menstruated during the month preceding the study. None of the women
in the study were using hormonal contraception or had ever been pregnant.
The women were blind to the hypotheses being tested and the identity of the
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# parental alleles matching each donor's alleles
P 0.0001
Fig. 3 Effects of inheritance and parental origin of HLA alleles on odor choice.
Number of allele matches between the paternally and maternally inherited
alleles of each woman (n=49) and the alleles of her most preferred odor donor,
compared with the number of matches with her least preferred donor. The
results of a three-factor repeated-measures analysis of variance were: interac-
tion of odor preference (most- versus least-preferred donor) ×parental origin
(paternal versus maternal alleles) ×inheritance (inherited versus not inherited
alleles) F(1,48)=11.16, P=0.002; interaction of odor preference ×inheritance
F(1,48)=11.63, P=0.001; main effect of odor preference F(1,48)=1.69, P=0.20;
main effect of parental origin F(1,48)=0.01, P=0.93; main effect of inheritance
F(1,48)=0.98, P=0.33.
© 2002 Nature Publishing Group http://genetics.nature.com
article
nature genetics •
volume 30 • february 2002
179
contents and odors of the boxes. The six male odor donors, derived from
Ashkenazi Jewish, Dutch, English, German, Polish, Scottish, Sikh and Spanish
ancestry, ranged in age from 23 y to 47 y (average 31.3 ± 3.8 y).
Odor collection. Male donors each wore three T-shirts; each shirt was
worn for two consecutive nights. The T-shirts and bedding were washed
with fragrance-free detergent. During the study period donors avoided a
list of 21 foods, including garlic and asparagus, and filled out a diet log.
We encouraged them to follow a bland diet similar to that of the isolated
community. Men showered with Ivory soap before putting on T-shirts
and refrained from using scented products such as deodorant, lotion,
cologne and aftershave. They also were instructed to avoid scents such as
cigarette smoke and pets as well as sexual activity or contact with other
individuals during odor collection. Men stored shirts of consecutive wear
in open plastic bags during the day. After the second night, we cut each T-
shirt in half with sterilized scissors, placed them in separate freezer con-
tainers and stored them at –80 ºC to prevent degradation of the
chemosignals. We kept shirt halves frozen until the morning of the olfac-
tory sessions. These procedures were approved by the Institutional
Review Board of the University of Chicago.
Olfactory sessions. Before each session, we put portions of the donor T-
shirts in unmarked cardboard boxes lined with foil, with a triangular hole
through which subjects smelled the contents. Subjects placed their noses in
the hole but could not see the contents of the box. Control T-shirts were
from the same stock, washed in the same fragrance-free detergent and pre-
sented in the same box type as worn T-shirts. The controls thus differed
only in their lack of additional human or household odors. We lined all
boxes with foil wrap to decrease box cardboard odor, to create a replaceable
lining around the triangular hole for hygiene and to prevent odor contam-
ination by the smellers. Each woman was asked to rate ten odor boxes (six
T-shirts from different male donors, one shirt with chlorine bleach, one
shirt with clove oil and two unworn shirt controls). Two male testers from
outside the community and blind to our specific hypotheses followed a
protocol with scripted questions. They presented boxes and recorded
women’s responses to the odors. Women held the boxes so that the nose
and chin were in the triangular opening of the box and, taking their time,
smelled the contents with active nasal inspirations. They verbally stated a
rating for each box, on the basis of a rating scale. The scale for both famil-
iarity and intensity ranged from zero to ten, with zero representing unfa-
miliar or undetectable odors and ten very familiar or very intense odors.
The scale for pleasantness and spiciness ranged from –5 to 5, with –5 repre-
senting very unpleasant or bland odors, and 5 representing very pleasant or
spicy odors. Ratings were standardized by z-score relative to ratings of the
carrier odor (freshly laundered T-shirts in a cardboard box).
For the odor choice test, the women smelled repeatedly three identical
boxes containing T-shirts; we then asked which odor they would choose to
smell all the time and which odor they would avoid. Choices were deter-
mined in two counterbalanced rounds that included all six donors. Then,
without knowing that they had previously chosen the odors, they were
asked to choose between the two boxes chosen in the previous rounds and
between the two boxes avoided in the previous rounds. Each woman thus
chose from all the donors her most preferred odor and her least preferred
odor, without knowing that they were male body odors.
HLA typing and scoring. We typed odor donors and subjects for HLA-A, -B,
-C and -DR antigens by serology, and –DQB1 alleles using molecular tech-
niques (Fig. 1)22. We determined matching scores for each female
smeller/male donor pair by counting the number of alleles present in the
male donor that matched an allele in the female. Homozygous alleles in the
smeller that matched a donor allele were counted as two matches. At the five
loci, there was a potential for a maximum of ten matches.
Acknowledgments
We thank D. Hayreh and P. Klimczyk for assistance on field trips, K. Beaman
for serological HLA typing the donors in this study, C. Wedekind for sharing
unpublished protocols and J. Brown for helpful comments. This work was
supported by a MERIT Award from the National Institute of Mental Health,
a grant from the John T. and Catherine D. MacArthur Foundation (to
M.K.M.), a grant from the National Institute of Child Health and
Development (to C.O.) and an MD/PhD Training Grant from the National
Institutes of Health (to S.J.).
Received 7 June; accepted 21 December 2001.
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Evidence from studies in rodents suggests that mate selection is influenced by major histocompatibility complex (MHC) haplotypes, with preferences for dissimilar partners. We initiated studies to determine whether avoidance of a mate with the same HLA haplotype as one’s own might be occurring in the Hutterites, a reproductive isolate of European origins. Previously, we reported a statistically significant deficiency of couples matching for 1 or more haplotypes among 411 couples with known HLA haplotypes defined by serology (Ober, Weitkamp, Cox, Dytch, Kostyu, & Elias, 1997). In this report, matching for 5-lo-cus, 11-locus and 16-locus HLA haplotypes defined by serological, molecular, and biochemical methods, we considered the same 411 couples. Using the same two methods for estimating the number of couples expected to match for a haplotype as we did in our earlier report, fewer couples than expected matched for a haplotype (first method, using population genotype frequencies, P = 0.0023-0.0035; second method, using computer simulations, P = 0.001-0.049). These results are consistent with the conclusion that Hutterite mate choice is influenced by HLA haplotypes, with an avoidance of spouses with haplotypes that are the same as one’s own.
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