Dr.Mercury
10-24-2005, 07:18 PM
Review
Human pheromones and sexual
attraction
Karl
Grammera,
Bernhard
Finka,[/
font]*, Nick
Neaveb
aLudwig–Boltzmann-Institute for Urban Ethology, c/o Institute of
Anthropology, University of Vienna, Althanstrasse 14, A-1090 Vienna,
Austria
bHuman
Cognitive Neuroscience Unit, School of Psychology and Sport Sciences, Northumbria University, Newcastle upon Tyne,
NE1 8ST, UK
Received 30 April 2004; accepted 19 August
2004
Abstract
Olfactory communication is very common amongst animals, and since the discovery of an accessory olfactory
system in humans, possible
human olfactory communication has gained considerable scientific interest. The
importance of the human sense of smell has by far been
underestimated in the past. Humans and other primates have
been regarded as primarily ‘optical animals’ with highly developed powers of
vision but a relatively undeveloped
sense of smell. In recent years this assumption has undergone major revision. Several studies indicate
that
humans indeed seem to use olfactory communication and are even able to produce and perceive certain
pheromones; recent studies have found
that pheromones may play an important role in the behavioural and
reproduction biology of humans. In this article we review the present
evidence of the effect of human pheromones
and discuss the role of olfactory cues in human sexual
behaviour.
# 2004 Elsevier
Ireland Ltd. All rights reserved.
Keywords:
Pheromone; Human; Sexual attraction; Mate preferences; Menstrual cycle; Oral
contraception
1.
Introduction
The importance of pheromones in intra-species
communication
has long been known in insects. A classical example
is bombykol, the sexual attractant of the
butterfly Bombyx
mori. Bombykol is
produced by the female butterflies in
odour glands of the abdomen. Male butterflies detect the
pheromone with
sensory cells, located in the antennae and
can find the females by the gradient of her odour. As little as
one
molecule of bombykol is enough to stimulate the
receptor cells and facilitate the orientation reaction.
Several
studies suggest that pheromones play an important role also
in mammalian social behaviour and thus in
humans as
well.
www.elsevier.com/locate/ejogrb
European
Journal of Obstetrics & Gynecology and
Reproductive Biology 118 (2005) 135–142
* Corresponding author. Tel.:
+43 1 4277 54769; fax: +43 1 4277
9547.
0301-2115/$
– see front matter # 2004 Elsevier Ireland
Ltd. All rights
reserved.
doi:10.1016/j.ejogrb.2004.08.010
The present
article reviews the current evidence how
pheromones
influence human life and interactions
and
discusses the consequences for human sexual attraction
and
mate-choice.
1.1.
Smell
According toKohl et al.
[1] the sense
of smell has largely
been underestimated in reproductive behaviours and it has
long been assumed that humans
are
‘microsmatic’ (poor
smellers) and rely essentially on visual and verbal
cues
when assessing potential mates. Certainly visual stimuli
play a key role in the perceptions of others
within a
sociosexual context, especially at a distance, but when
individuals get closer and personal intimacy
is increased, it
is likely that smell also plays a key role a variety of
sociosexual behaviours. Recent
studies have indeed
suggested that olfaction (conscious and unconscious)
can play a
significant role in human reproductive
biology.
Zajonc’s
[2]
‘affective
primacy’ hypothesis states that
both
positive and negative affect can be evoked with minimal
stimulus input and only minor cognitive
involvement.
Olfactory signals induce emotional responses even if an
olfactory stimulus is not consciously
perceived: this is due
to the fact that olfactory receptors not only send projections
to the neocortex for
conscious processing (e.g. the nature of
a particular aroma) but also to the limbic system for
emotional
processing (e.g. memories and affect associated
with a particular
smell).
1.2.
Pheromones
The term
‘pheromone’ was introduced by Karlson and
Luscher
[3] and it
derives from the Greek words
‘pherein’
(to carry) and
‘hormon
’ (to excite). Pheromones are referred
to as
‘ecto-hormones’ as they are chemical messengers that
are emitted into the
environment from the body where they
can then activate
specific physiological or
behavioural
responses in other individuals of the same species.
According to McClintock
[4] pheromones
can be divided
into two classes. Firstly,
‘signal
pheromones’ produce
shortterm
behavioural changes and seem to act as attractants and
repellents. Secondly,
‘primer
pheromones’ produce
longerlasting
changes in behaviour via their activation of
the
hypothalamic–pituitary[/
font]–adrenal (HPA) axis
[4]. In
particular,
it is assumed that primer pheromones trigger the
secretion of GnRH from the hypothalamus, which in
turn
triggers the release of gonadotropins (LH, FSH) from the
pituitary gland. These gonadotropins
influence gonadal
hormone
secretion, e.g. follicle maturation in the ovaries in
females, testosterone and sperm production in males.
In
support, in various species the short-term exposures of
females to males have been associated with a
corresponding
rise in testosterone
[5]. Four
specific functions of
pheromones
have been determined: opposite-sex attractants,
same-sex repellents,
mother–infant bonding attractants
and
menstrual cycle modulators
[6]. It is the
first category that
this review
will focus upon though may draw upon evidence
from the other categories wherever
relevant.
1.3. Pheromone
detection
In most mammals, a specialised region of the
olfactory
system called the vomeronasal organ (VNO), also referred to
as
‘Jacobson’s organ’
is responsible for pheromone
detection. The principal evidence that the
VNO plays a
role in mammalian pheromone detection comes from lesion
studies where removal of the VNO produces
reliable
impairments in reproductive behaviours
[7]. The VNO
is
located above the hard palate on both sides of the nasal
septum and it is lined with receptor cells whose
axons
project to the accessory olfactory bulb, which sends its
projects to the hypothalamic nuclei
[8]. Pheromones
can
thus potentially influence
sexual and reproductive behaviours
and endocrine function via the HPA axis
[9].
There
has been some scepticism concerning the ability of humans
to detect and respond to pheromones due to the
facts that
VNO appears to vestigial in some primates, and the
accessory olfactory bulb is not discernable in
humans
[9].
However
, it has since been reported that humans do
possess a functional VNO that responds to pheromones
(even in
picogram amounts) in a sex-specific
manner
[10–12][f
ont=AdvP41153C]. Recently, the
identification of a
pheromone
receptor gene expressed in human olfactory mucosa has
further strengthened the case for a
functioning VNO
[13].
Furthe
r evidence comes from patients with
Kallmann’s
syndrome, which occurs
due to the underdevelopment of
the olfactory bulb in the embryo and minimal GnRH
secretions from the
hypothalamus. Individuals have
underdeveloped gonads, lack secondary sexual characteristics,
are anosmic, and
preliminary research indicates that
they show no response to pheromones (personal communication
cited in
[1]).
n
1.4. Pheromone
production
The main producers of human pheromones are
the
apocrine glands located in the axillae and pubic region. The
high concentration of apocrine glands found
in the armpits
led to the term
‘axillary
organ’, which is considered
an
independent
‘organ[
size=2]’ [/size]of human odour production. Apocrine
glands develop in the embryo,
but become functional only
with the onset of puberty. At sexual maturation, they
produce steroidal secretions
derived from 16-androstenes
(androstenone and androstenol) via testosterone, and as
such, the concentrations
of several 16-androstenes
is
significantly higher in males
[14]. Freshly
produced
apocrine secretions are odourless but are transformed into
the odorous androstenone and androstenol
by aerobic
coryeform bacteria
[15]. In the
vagina, aliphatic acids
(referred to as copulins) are secreted and their odour varies
with the menstrual cycle
[16]. It is now
possible to isolate
K. Grammer
136 et al. / European Journal of
Obstetrics & Gynecology and Reproductive Biology 118 (2005)
135–142
and manufacture synthetic human pheromones and such
compounds are often used in research
as they are relatively
easy to make, convenient to store, and easy to
apply.
1.5. Pheromone effects on animal
reproductive
behaviours
Preliminary studies in the 1960s
demonstrated that
exposure to boar odour elicited the mating stance in females.
Subsequent experiments showed
that application of male
urine or semen to the
female’s snout also produced the
same
effect. Studies have appeared to demonstrate a number
of
confirmed effects of pheromones
in animals. Firstly
the
‘Lee-Boot
Effect’ [17]
describes the effects of the social
environment on the female
reproductive cycle. The authors
noted that when female mice were housed 4 in a cage their
oestrous cycles
became synchronised and extended.
Secondly, the
‘Whitten
effect’ [18]
confirmed that female
mice housed together displayed an extended oestrous cycle,
but further noted
that when a male was introduced the
females ovulated synchronously
3–4 days later. The
substance was
found to be androgen-based pheromones
secreted in the
male’s urine.
Thirdly, the
‘Bruce
effect’ [19]
describes the effect of
housing pregnant mice with males that were
not their
original mates. Within 48 h of such pairings,
significantly
more miscarriages
were observed in the females. Subsequent
mating with the new male within
3–6 days then always
followed the
failed pregnancy. The inclusion of castrated or
juvenile male strangers had no such effects. This appears
to
be a male tactic of blocking the pregnancy by a previous
male and bringing the female quickly into
oestrous. Finally
the ‘Vandenburgh
effect’ [20]
notes that young female rats
exposed to adult males for 20 days
after weaning entered
puberty earlier than female pups not exposed to males. Male
pheromones stimulate
puberty, probably by releasing LH,
which stimulates follicular growth, presumably so that they
can mate
earlier. A related effect was noted in that female
mice housed alone attain puberty earlier than female
mice
housed together, females can thus delay puberty in
their
conspecifics, probably by
suppressing LH and FSH release
from the anterior pituitary
gland.
1.6. Pheromones and human reproductive
behaviours
Several authors have speculated that pheromones
may
influence human sociosexual
behaviours (e.g.
[21,22])
and
evidence for the effects of putative pheromones on human
sexual behaviours has come from several
sources:
1. Human correlates of animal effects
McClintock
[23] reported
that human female college
students demonstrated synchrony in their menstrual
cycles when housed in shared
accommodation (Lee–Boot
effect).
Preti et al. [24]
extended this research by applying
extracts of female sweat to the
upper lips of female
volunteers three times per week for 4 months. At the end
of this time the participants
showed significantly
greater
menstrual synchrony than volunteers in a control group.
Cutler et al.
[25] also
showed that the application of male
axillary secretions to the upper lips of female volunteers
also had a
regulatory effect on the menstrual cycle
(Whitten effect). Ellis and Garber
[26] showed
that girls
in stepfather-present homes experienced faster puberty
than girls in single-mother homes, the
younger the
daughter when the new male arrived on the scene then the
earlier her pubertal maturation
(Vandenburgh effect).
2. Laboratory studies
In an early report, Kirk-Smith et al.
[27] asked 12
male
and female undergraduates to rate photographs of people,
animals and buildings using 159-point bipolar
scales
(e.g.
unattractive–attractive),
while wearing surgical masks
either impregnated with androstenol or left undoctored.
Mood ratings were also
completed. In the presence of
androstenol, male and female stimuli were also rated as
being
‘warmer
’ and
‘more
friendly’. Van Toller et al.
[28]
showed that skin conductance in volunteers exposed to
androstenone was higher than that of
non-exposed
volunteers thereby providing evidence as to the
physiological effects of pheromone exposure.
However,
Benton and Wastell [29]
had groups of females read
either a neutral or a sexually arousing
passage whilst
exposed to either androstenol or a placebo substance.
While sexual arousal was higher in the
‘arousal’
condition, the authors found no evidence that
exposure
to androstenol had
influenced sexual
feelings.
Filsinger et al. [30]
asked males and females to rate
vignettes of a
fictional target male and female
using
semantic differentials, and also to provide a selfassessment
of mood. The test materials had been
sealed
into plastic bags, which were either impregnated with
androstenol, androstenone, a synthetic musk
control, and
a no-odour control. Females exposed to androstenone
produced lower sexual attractiveness ratings
of the target
male, while males exposed to androstenol perceived the
male targets to be more sexually
attractive.
The interpretation from such studies is further
complicated by two factors. Firstly, female
olfactory
sensitivity is moderated by the menstrual cycle with
smell sensitivity peaking at ovulation
[31]. Benton
[32]
reported that androstenol application
influenced ratings
of subjective
mood at ovulation, and Grammer [21]
found
that females rated androstenone differently at
various
phases of their menstrual cycle. Secondly, the use of oral
contraception may affect smell sensitivity
and gonadal
hormone levels thereby possibly disrupting pheromone
detection. Use of the contraceptive pill does
indeed
appear to influence female
perception of
androstenone
[21].
More recently Thorne et al. [33]
employed a repeatedmeasures,
double blind, balanced crossover
design to
assess the possible
influence of menstrual cycle
phase
K. Grammer et al. / European Journal of Obstetrics &
Gynecology and Reproductive Biology 118 (2005)
135–142
137
and contraceptive
pill use. Sixteen pill and non-pill users
were tested during both menses and mid-cycle in
both
pheromone-present and pheromone-absent conditions.
During each session (four in all) the volunteers rated
male
vignette characters, and photographs of male faces, on
various aspects of attractiveness. Pheromone
exposure
resulted in significantly
higher attractiveness ratings of
vignette characters, and faces. Use of the contraceptive
pill or menstrual
cycle phase had equivocal effects on
some vignette items but neither had any
influence on
female ratings of male
facial attractiveness.
Not all laboratory studies have found positive results
however (e.g.
[34]), and some
authors are sceptical that
higher primate reproductive behaviours are
significantly
influenced by pheromones
[35]. Thus,
while the current
scientific
opinion regarding the existence of human
pheromones remains positive, opinion remains divided as
to whether
such substances do in fact influence
human
sociosexual behaviours. This is probably due to the fact
that while a wealth of laboratory-based studies
has been
conducted, very different methodologies mean that
comparisons between studies are
difficult.
Furthermore,
methodologically solid double blind, placebo-controlled,
crossover studies are few and far
between, the Thorne et
al. [33]
study being an exception. However, that study
was laboratory based
and simply required participants to
rate the attractiveness of hypothetical opposite-sex
characters based on
written descriptions and photographs.
The ecological validity of such laboratory-based
studies is therefore
questionable.
3. Real-life studies
While laboratory studies are able to exert more control
over the varying
factors involved, of potential greater
relevance are studies assessing the effects of pheromones
in real-life
situations. Early studies were, however, not
promising. For example, Morris and Udry
[36]
prepared
aliphatic acid smears, formulated to mimic
concentrations
shown to be effective in enhancing monkey
reproductive behaviour. The solution was smeared
on
the chests of 62 married women on eight randomly
assigned nights through three menstrual cycles.
Volunteers
did not report any increase in sexual intercourse on
these test nights. However, Cowley and
Brooksbank
[37]
asked males and females to wear a necklace either
containing an opposite-sex pheromone or a
control
substance while they slept. The next day, they found that
women who had worn the male pheromones in
their
necklace reported
significantly more interactions
with
males than the control group.
Two studies which have often been cited as the
strongest evidence yet
provided for the influence
of
pheromones on human sociosexual behaviour are those
of Cutler et al.
[38] and McCoy
and Pitino
[39].
Both
studies employed double blind, placebo-controlled
methods and focussed upon the effects of
synthetic
pheromones on self-reported sociosexual behaviours in
young men
[38] and women
[39]. In the
first study
[38] 38
male
volunteers recorded the occurrence of six sociosexual
behaviours (petting/affection/kissing; formal
dates;
informal dates; sleeping next to a partner; sexual
intercourse; and masturbation) over a 2-week
‘baseline’
period. Over the next 6 weeks the volunteers kept
the
same records while daily applying a male pheromone or a
control substance added to their usual aftershave
lotion.
The authors reported that a
significantly higher proportion
of
pheromone users compared to placebo users
showed an increase from baseline in
‘sexual
intercourse’
and
‘sleeping next to a romantic
partner’. In general 58%
of the
pheromone group compared to 19% of the placebo
group showed increases in two or more behaviours
compared to
baseline; 41% of the pheromone group
compared to 9.5% of the placebo group showed increases
in three or more
behaviours compared to baseline.
In the second study [39]
36 female volunteers recorded
the occurrence of the same six
socio-sexual behaviours and
an additional behaviour
‘male
approaches’ over a
2-week
‘baseline[/size
]’ period. Over the next 6 weeks they then
either
applied a synthetic female pheromone or a control
substance added to their usual perfume on a daily
basis.
While the groups did not differ in their sociosexual
behaviours at baseline, a
significantly higher proportion
of
the pheromone group showed increases in the following
behaviours:
‘sexual
intercourse’,
‘sleeping next to
a
partner’,
‘formal
dates’ and
‘[font=AdvP41153C]petting/affection/kissing[/fon
t]’.
However, as pheromone exposure can shift the
timing of
ovulation, the authors recalculated the data to only include
the
first experimental cycle. After these
recalculations the
pheromone group only
significantly differed from
the
placebo group in ‘sexual
intercourse’ and
‘formal
dating’.
In terms of percentages,
three or more sociosexual
behaviours increased over baseline in 74% of pheromone
users but only 23% of placebo
users. As there was no
increase in self-reported masturbation the authors argued
that the changes did not
reflect changes in
sexual
motivation, but that the pheromones had
‘‘positive sexual
attractant
effects. . .’’
(p. 374).
The results of these studies appear to provide
impressive
evidence for the effects of synthetic pheromones
on sexual attractiveness. However, there are a
number of
methodological problems with the studies,
which make the
findings less emphatic. Firstly,
the
studies did not control for the attractiveness of the
volunteers nor make allowance for this when
allocating
the conditions. If for example the pheromone groups had
contained slightly more attractive
individuals than the
control groups, then subsequent positive effects attributed
to pheromones may be
misleading. Secondly, all the
data were of the self-report kind (prone to error and
subjective bias especially
as
‘back[s
ize=2]filling’
was allowed in
the second study) and as such no objective record of
the
putative effects of pheromone versus placebo were
obtained. Thirdly the groups differed widely in terms
of
K. Grammer 138
et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology
118 (2005)
135–142
their dating status with some being married, some in
long-term relationships and others
being single. Those in
relationships would have certainly recorded more of
certain sociosexual behaviours than
the single volunteers,
it would have been better if the entire subject pool were
single males seeking more
dating/sex opportunities.
Fourthly, the baseline period of 2 weeks is
difficult to
equate with a testing
period of 6 weeks even though
average differences from baseline were analysed. How
can we be sure that the
social behaviour of the volunteers
changed not as a result of pheromone exposure but by
other factors during
the experimental period, e.g. going
on holiday, celebrating at an
office party? While the
actual
behaviours were recorded, the context within
which those behaviours occurred was not controlled for.
The
evidence from these two studies thus indicates
that certain sociosexual behaviours are increased in
males and
females who wear pheromones, compared to
baseline. However, the studies do not convincingly show
that the
pheromone and placebo groups were well
matched; that the baseline and experimental conditions
were matched in
terms of various temporal and
behavioural factors; that objective changes in sociosexual
behaviours did occur;
and that the pheromones served as
a
‘sexual
attractants’ rather than say a mood
enhancer,
confidence builder,
etc.
4. Genetic signalling
Various
‘good
genes’ theories of sexual selection
have
emphasised the importance of
immunocompetence
[40,41]
in that females can obtain good genes for their
offspring by
mating with males whose genes are
complementary to their own. A possible mechanism
by which this can be
achieved is via body odour. The
major histocompatibility complex (MHC) is a large
chromosomal region
containing closely linked polymorphic
genes that play a role in immunological self/
non-self recognition; this
genetic information is relayed
by androgen-based pheromones
[42]. Numerous
studies
in rodents have now established that MHC genotype is
involved in odour production, and such odours are
used in
individual discrimination
[43]. House
mice learn the
MHC identity of their family during development and
avoid mating with individuals carrying
familial MHC
genes; they do so through the use of odour cues from
urine (e.g.
[44,45]). Is
there any evidence that humans
possess these abilities?
Some studies have shown that women seem to
prefer
the odours of immunocompatible men. Wedekind et
al.
[46]
HLA-typed (Human Leukocyte Antigen is the
human MHC) 49 women and
44 men and asked the
women to rate the attractiveness of the odours of t-shirts
worn by three MHC-similar and
three MHC-dissimilar
men.Women rated the odour of the MHC-dissimilar men
as
‘more
pleasant’, and this odour was
significantly more
likely to remind
them of their own mate’s
odour.
Interestingly, the preferences of women taking an oral
contraceptive were
reversed—they preferred the
MHCsimilar
odours. This could be due to the fact that oral
contraceptives mimic the effects of pregnancy,
and
pregnant females may be attracted to MHC-similar
individuals who are likely to be close kin and
potential
reproductive helpers.
In a similar study, Thornhill and Gangstad
[47]
measured bilateral physical traits in males and females
and then asked the volunteers to wear the same
T-shirt for
two consecutive nights. Opposite-sex participants then
rated the shirts for
‘pleasantness’,
‘sexiness’
and
‘[fo
nt=AdvP41153C]intensity’;
donor’s facial attractiveness was
also
assessed by different opposite-sex volunteers. Non-pill
users in the fertile phase of their menstrual
cycle gave the
T-shirts worn by symmetrical males higher ratings; this
was not seen in females using the
contraceptive pill, or in
females at unfertile phases of their cycle. Female
symmetry had no
influence on male ratings. The
authors
proposed that the so-called
‘scent of
symmetry’ is an
honest indicator of
male genetic quality.
In a real-life study of actual mate choices, Ober et
al.
[48]
found evidence for HLA-dependent mate preferences
in a population
of Hutterites (a small, genetically
isolated religious sect). They found that couples were less
likely to
share MHC haplotypes than chance, and in
couples that had a similar MHC they demonstrated
unusually long
inter-birth intervals (unconscious avoidance
of inbreeding?).
Milinski and Wedekind
[49] HLA-typed
males and
females and then asked them to smell 36 scents
commonly used in perfume/aftershave. They rated
each
scent on whether they liked it or not, and whether they
would use it on themselves. The authors reported
a
significant correlation between
HLA and scent scoring
for themselves but not for others, showing the people
unconsciously select perfumes to
enhance their own body
odours that reveal their genetic
make-up.
1.7. Pheromones and the battle of the
sexes
Differential parental investment theory
[50] predicts
that
when looking for long-term relationships females should
seek out and choose males who are ready to invest
resources
in their offspring. This minimizes female investment, but
maximizes overall investment through added
male assistance.
In contrast, males are expected either to attempt
copulation frequently and with as many
fertile females as
possible, or to develop a long-term pair bond. This helps to
ensure that either a large
number of offspring survive
without
significant paternal investment, or
that male parental
investment occurs primarily when another male does not
father offspring.
According to
this theory, it is adaptive for females and
males to develop and use cognition in mate selection, which
takes
into account biological constraints. Thus, mate
selection is a task of information processing, and
evolution
K. Grammer et al. / European Journal of Obstetrics
& Gynecology and Reproductive Biology 118 (2005)
135–142
139
would have
favoured individuals who were able to quickly
and reliably process information that allowed them to
make
appropriate mating decisions. Adaptive cognition could be
expected to lead to optimal decision-making
under a wide
spectrum of socio-economic constraints. The existence of
ubiquitous sex
specific differences in mate selection
criteria
[51]
attests that male and female cognition is adapted to
the
biological constraints of mate selection.
Neither males nor females can perceive ovulation in
humans
consciously. This is surprising in the light of the fact
that it has been shown to be associated with a number
of
overt physiological and behavioural changes. One
‘unconscious’
mechanism associated with these menstrual
cycle
changes might be that of olfactory perceptions.
Alexander and Noonan
[52], and
Symons [53]
have
argued that hidden oestrous has evolved because
females
need to trick males into forming a bond. Males unaware
of
female’ s fertility would remain
bonded to ensure
impregnation and paternity. A female providing clues to
her ovulation might risk losing male
investment, due to
paternal uncertainty and the limited temporal reproductive
interaction. This development
would implicate the male fear
of cuckoldry as an evolutionary pressure
[50]. The
outcome
would be that the female’s
ability to secure paternal care is
affected by mechanisms that increase temporal aspects of
the pair bond and
enhance male confidence of
paternity.
In contrast with this line of argument, Benshoff and
Thornhill
[54] and Symons
[53] have
proposed a second
evolutionary scenario in which hidden oestrous evolved to
increase the chances of successful
cuckoldry by females so
they ‘‘can
escape the negative consequences of being pawns
in marriage games’’
([55]
p. 350). Once monogamy is
established, a
female’s best strategy would be to
copulate
outside the pair bond because she can then obtain superior
genes with a certain expectation of
paternal investment. In
this case the outcome is genetically superior offspring.
These two hypotheses imply
different impacts of
heritable traits. If those genes which induce paternal care
were relevant for offspring
success, a male paternitysecuring
function for lost oestrous would be possible. If
there are other relevant
traits not related to paternal care but
relevant to offspring survival, then hidden oestrous could
allow
females to exploit occasional opportunities to mate
outside the pair bond
[56]. In both
cases, male knowledge of
ovulation may be selected against because it would hinder
the
female’s mating strategies
[52,57].
Rec
ently, the second hypothesis has received considerable
support. Bellis and Baker
[58] conducted
a study of
2708 females and found those 13.8% of 145
‘unprotected’
extra-pair copulations (EPC) occurred during
the fertile
period and were preceded in most cases by intra-pair
copulations (IPC). EPCs were rarely followed
by IPCs.
According to his study EPC and thus female
infidelity peaks
at ovulation. The
authors conclude that these results hint at
female-induced sperm competition, which would be
expected by the
second hypothesis of the evolutionary
function of concealed ovulation discussed above. Still it is
unclear
what proximate mechanism or mechanisms cue
female EPC at ovulation. The assumption that concealed
ovulation
serves to deceive males is common to all these
theories. Supposedly, females deceive males about the
fertile
phase of the menstrual cycle to help ensure male parental
investment, which yields an optimal number
of offspring.
Additionally, concealed ovulation helps females to monopolize
reproduction and, as a
consequence, forces males to
develop reproductive strategies for gaining access to
ovulating females. It is
reasonable to expect male counter
strategies would develop against the deceptive attempt by
females to conceal
ovulation. Grammer [21]
described a
possible male counter strategy: the evolution of
the
androstenone–androstenol
signalling system. In his study,
290 female subjects rated the odour of androstenone. A
change in assessment
throughout the menstrual cycle was
found: at the time of ovulation the women found the scent of
androstenone,
the most dominant odour of the male armpit,
to be more pleasant than on the other days of the menstrual
cycle.
These results suggest that there is a change in the
emotional evaluation of males triggered by the reaction
to
androstenone. The findings
support previous results by
Maiworm
[59], which
were of borderline significance.
Male
body odour is usually perceived as unattractive and
unpleasant by females but this evaluation changes at
the
point in the menstrual cycle when conception is most likely.
This
finding is underlined by the fact that
anosmia to
androstenone also varies with cycle. At the conceptual
optimum we
find fewer anosmic females. It could
be
suggested that changes in anosmia during the cycle could
also be a female strategy, although more data need
to be
gathered to prove this hypothesis. Thus the change in female
attitudes towards male body odour could
have a strong
impact on mate selection and perhaps self-initiated
copulations by females. If we regard the
androstenol–
androsten
one-signaling system, the situation for androstenol
seems clear, it makes males more attractive for
females.
Female advantage in this case is nil, unless
fitter males
produce more
androstenol. The situation is more complicated
because producing androstenol inevitably produces
androstenone.
The androstenone production has a disadvantage
in its unpleasantness. Hence
attractiveness-enhancing
androstenol immediately oxidizes to androstenone,
which repels females. A
non-producing male could do quite
well in a population of producers, because females would
not be repelled by
his body odour. So the attractivenessenhancing
component of the smell does not seem to be the
main, or at
least only, function of the signalling system.
Regarding androstenone, the fact that females assessed
its
odour as more pleasant at the time of ovulation could be of
advantage for males, as odorous males will be
more
successful when approaching ovulating females, rather than
non-ovulating females. This suggests that
males use a kind
of passive
‘ovulation-radar’ for the detection of the actually
hidden
ovulation.
K. Grammer
140 et al. / European Journal of
Obstetrics & Gynecology and Reproductive Biology 118 (2005)
135–142
Females faced with an evolved male strategy to detect
hidden ovulation would be likely
to develop a counter
strategy. One possible strategy could be to manipulate male
cognition and thus adaptive
male information processing in
mate selection. Research on many species of non-human
primates (especially on
rhesus monkeys) has shown the
ability to perceive ovulation by smell. Although normally
motivated to copulate,
when sexually inexperienced rhesus
males were made anosmic they showed no further sexual
motivation despite a
powerful visual cue: the
female’s
swelling
[60].
Furthermore, rhesus males show no interest in
ovariectomized rhesus females, presumably because
ovariectomized
rhesus females lose the odour characteristic of
ovulation. Rhesus males regain interest in
copulation when
the vaginal secretions from non-ovariectomized females are
applied to ovariectomized females.
Studies on menstrual
cycle
fluctuations in the fatty-acid
composition of women’s
vaginal
fluids indicated that a similar type
of signalling
system might also exist in humans [16,
61–[col
or=#000066]63][/color]. For example,
human vaginal secretions have a
composition that is similar
to the vaginal secretions of female rhesus monkeys. The
application to
ovariectomized female rhesus monkeys, either
of human, or rhesus vaginal secretions, induced
similar
activation of rhesus male sexual interest
[64].
The
behaviourally active fraction of the rhesus
vaginal
secretions—referred to as
‘Copulins’—consists of volatile,
short-chained fatty acids
[65]. These
same substances (i.e.,
the short-chained fatty acids: acetic, propanoic, butanoic,
methylpropanoic,
methylbutanoic, methylpentanoic acid)
occur in human vaginal secretions, albeit in slightly different
amounts
[16]. In
addition, the composition of these copulins
varies during the menstrual cycle
[62].
Cowley
et al. [66]
found that rhesus vaginal secretions
change
peoples’ assessment of other people,
and that the
application of copulins tends to yield a more positive
impression of females. Doty et al.
[67] used a
questionnaire
to evaluate the intensity and pleasantness of different
vaginal
fluids from a
complete menstrual cycle. They found that
odour at ovulation was both the most intense odour and the
least
unpleasant.
In a study by Juette (unpublished data) synthesized
female vaginal secretions
(‘Copulins’) were tested for their
ability to act as signals for males.
Menstrual, ovulatory and
pre-menstrual fatty acid compositions of Copulins and an
odourless water control were
presented to 60 non-smoking
male subjects for 25 min in a double-blind experiment. To
control for changes in
sex hormones that were induced by
copulins, saliva-samples were taken before and after presentation.
While
inhaling either a composition of copulins or a
control, males rated pictures of females for attractiveness.
It
was shown that ovulatory fatty acid compositions stimulated
male androgen secretion and changed the
discriminatory
cognitive capacities of males with regard to female attractiveness
in that males became less
discriminating. As we can
learn from the above examples, human pheromones seem to
work as beautifully balanced
‘strategic
weapons’ in
the
‘battle of the
sexes’ and the
‘war of
signals’ resulting from
asymmetric
investment theory.
2.
Conclusion
As we can learn from the reviewed studies
on
pheromones, the model of humans being only optical
animals has to be revised. Human sociosexual
interactions
are influenced by
pheromones, even if they cannot be
detected consciously. Pheromones have the potential
to
influence human behaviour and
physiology and so there has
to be asked the question, in which way the modern striving
for cleanliness and
odourlessness affects our everyday social
lives and human reproductive success in the future. What we
know at
the moment, as many studies in the last few years
have pointed out, is that the human sense of smell has by
far
been underestimated in the past and that humans, like other
animals, use olfactory signals for the
transmission of
biologically relevant
information.
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135–142
Human pheromones and sexual
attraction
Karl
Grammera,
Bernhard
Finka,[/
font]*, Nick
Neaveb
aLudwig–Boltzmann-Institute for Urban Ethology, c/o Institute of
Anthropology, University of Vienna, Althanstrasse 14, A-1090 Vienna,
Austria
bHuman
Cognitive Neuroscience Unit, School of Psychology and Sport Sciences, Northumbria University, Newcastle upon Tyne,
NE1 8ST, UK
Received 30 April 2004; accepted 19 August
2004
Abstract
Olfactory communication is very common amongst animals, and since the discovery of an accessory olfactory
system in humans, possible
human olfactory communication has gained considerable scientific interest. The
importance of the human sense of smell has by far been
underestimated in the past. Humans and other primates have
been regarded as primarily ‘optical animals’ with highly developed powers of
vision but a relatively undeveloped
sense of smell. In recent years this assumption has undergone major revision. Several studies indicate
that
humans indeed seem to use olfactory communication and are even able to produce and perceive certain
pheromones; recent studies have found
that pheromones may play an important role in the behavioural and
reproduction biology of humans. In this article we review the present
evidence of the effect of human pheromones
and discuss the role of olfactory cues in human sexual
behaviour.
# 2004 Elsevier
Ireland Ltd. All rights reserved.
Keywords:
Pheromone; Human; Sexual attraction; Mate preferences; Menstrual cycle; Oral
contraception
1.
Introduction
The importance of pheromones in intra-species
communication
has long been known in insects. A classical example
is bombykol, the sexual attractant of the
butterfly Bombyx
mori. Bombykol is
produced by the female butterflies in
odour glands of the abdomen. Male butterflies detect the
pheromone with
sensory cells, located in the antennae and
can find the females by the gradient of her odour. As little as
one
molecule of bombykol is enough to stimulate the
receptor cells and facilitate the orientation reaction.
Several
studies suggest that pheromones play an important role also
in mammalian social behaviour and thus in
humans as
well.
www.elsevier.com/locate/ejogrb
European
Journal of Obstetrics & Gynecology and
Reproductive Biology 118 (2005) 135–142
* Corresponding author. Tel.:
+43 1 4277 54769; fax: +43 1 4277
9547.
0301-2115/$
– see front matter # 2004 Elsevier Ireland
Ltd. All rights
reserved.
doi:10.1016/j.ejogrb.2004.08.010
The present
article reviews the current evidence how
pheromones
influence human life and interactions
and
discusses the consequences for human sexual attraction
and
mate-choice.
1.1.
Smell
According toKohl et al.
[1] the sense
of smell has largely
been underestimated in reproductive behaviours and it has
long been assumed that humans
are
‘microsmatic’ (poor
smellers) and rely essentially on visual and verbal
cues
when assessing potential mates. Certainly visual stimuli
play a key role in the perceptions of others
within a
sociosexual context, especially at a distance, but when
individuals get closer and personal intimacy
is increased, it
is likely that smell also plays a key role a variety of
sociosexual behaviours. Recent
studies have indeed
suggested that olfaction (conscious and unconscious)
can play a
significant role in human reproductive
biology.
Zajonc’s
[2]
‘affective
primacy’ hypothesis states that
both
positive and negative affect can be evoked with minimal
stimulus input and only minor cognitive
involvement.
Olfactory signals induce emotional responses even if an
olfactory stimulus is not consciously
perceived: this is due
to the fact that olfactory receptors not only send projections
to the neocortex for
conscious processing (e.g. the nature of
a particular aroma) but also to the limbic system for
emotional
processing (e.g. memories and affect associated
with a particular
smell).
1.2.
Pheromones
The term
‘pheromone’ was introduced by Karlson and
Luscher
[3] and it
derives from the Greek words
‘pherein’
(to carry) and
‘hormon
’ (to excite). Pheromones are referred
to as
‘ecto-hormones’ as they are chemical messengers that
are emitted into the
environment from the body where they
can then activate
specific physiological or
behavioural
responses in other individuals of the same species.
According to McClintock
[4] pheromones
can be divided
into two classes. Firstly,
‘signal
pheromones’ produce
shortterm
behavioural changes and seem to act as attractants and
repellents. Secondly,
‘primer
pheromones’ produce
longerlasting
changes in behaviour via their activation of
the
hypothalamic–pituitary[/
font]–adrenal (HPA) axis
[4]. In
particular,
it is assumed that primer pheromones trigger the
secretion of GnRH from the hypothalamus, which in
turn
triggers the release of gonadotropins (LH, FSH) from the
pituitary gland. These gonadotropins
influence gonadal
hormone
secretion, e.g. follicle maturation in the ovaries in
females, testosterone and sperm production in males.
In
support, in various species the short-term exposures of
females to males have been associated with a
corresponding
rise in testosterone
[5]. Four
specific functions of
pheromones
have been determined: opposite-sex attractants,
same-sex repellents,
mother–infant bonding attractants
and
menstrual cycle modulators
[6]. It is the
first category that
this review
will focus upon though may draw upon evidence
from the other categories wherever
relevant.
1.3. Pheromone
detection
In most mammals, a specialised region of the
olfactory
system called the vomeronasal organ (VNO), also referred to
as
‘Jacobson’s organ’
is responsible for pheromone
detection. The principal evidence that the
VNO plays a
role in mammalian pheromone detection comes from lesion
studies where removal of the VNO produces
reliable
impairments in reproductive behaviours
[7]. The VNO
is
located above the hard palate on both sides of the nasal
septum and it is lined with receptor cells whose
axons
project to the accessory olfactory bulb, which sends its
projects to the hypothalamic nuclei
[8]. Pheromones
can
thus potentially influence
sexual and reproductive behaviours
and endocrine function via the HPA axis
[9].
There
has been some scepticism concerning the ability of humans
to detect and respond to pheromones due to the
facts that
VNO appears to vestigial in some primates, and the
accessory olfactory bulb is not discernable in
humans
[9].
However
, it has since been reported that humans do
possess a functional VNO that responds to pheromones
(even in
picogram amounts) in a sex-specific
manner
[10–12][f
ont=AdvP41153C]. Recently, the
identification of a
pheromone
receptor gene expressed in human olfactory mucosa has
further strengthened the case for a
functioning VNO
[13].
Furthe
r evidence comes from patients with
Kallmann’s
syndrome, which occurs
due to the underdevelopment of
the olfactory bulb in the embryo and minimal GnRH
secretions from the
hypothalamus. Individuals have
underdeveloped gonads, lack secondary sexual characteristics,
are anosmic, and
preliminary research indicates that
they show no response to pheromones (personal communication
cited in
[1]).
n
1.4. Pheromone
production
The main producers of human pheromones are
the
apocrine glands located in the axillae and pubic region. The
high concentration of apocrine glands found
in the armpits
led to the term
‘axillary
organ’, which is considered
an
independent
‘organ[
size=2]’ [/size]of human odour production. Apocrine
glands develop in the embryo,
but become functional only
with the onset of puberty. At sexual maturation, they
produce steroidal secretions
derived from 16-androstenes
(androstenone and androstenol) via testosterone, and as
such, the concentrations
of several 16-androstenes
is
significantly higher in males
[14]. Freshly
produced
apocrine secretions are odourless but are transformed into
the odorous androstenone and androstenol
by aerobic
coryeform bacteria
[15]. In the
vagina, aliphatic acids
(referred to as copulins) are secreted and their odour varies
with the menstrual cycle
[16]. It is now
possible to isolate
K. Grammer
136 et al. / European Journal of
Obstetrics & Gynecology and Reproductive Biology 118 (2005)
135–142
and manufacture synthetic human pheromones and such
compounds are often used in research
as they are relatively
easy to make, convenient to store, and easy to
apply.
1.5. Pheromone effects on animal
reproductive
behaviours
Preliminary studies in the 1960s
demonstrated that
exposure to boar odour elicited the mating stance in females.
Subsequent experiments showed
that application of male
urine or semen to the
female’s snout also produced the
same
effect. Studies have appeared to demonstrate a number
of
confirmed effects of pheromones
in animals. Firstly
the
‘Lee-Boot
Effect’ [17]
describes the effects of the social
environment on the female
reproductive cycle. The authors
noted that when female mice were housed 4 in a cage their
oestrous cycles
became synchronised and extended.
Secondly, the
‘Whitten
effect’ [18]
confirmed that female
mice housed together displayed an extended oestrous cycle,
but further noted
that when a male was introduced the
females ovulated synchronously
3–4 days later. The
substance was
found to be androgen-based pheromones
secreted in the
male’s urine.
Thirdly, the
‘Bruce
effect’ [19]
describes the effect of
housing pregnant mice with males that were
not their
original mates. Within 48 h of such pairings,
significantly
more miscarriages
were observed in the females. Subsequent
mating with the new male within
3–6 days then always
followed the
failed pregnancy. The inclusion of castrated or
juvenile male strangers had no such effects. This appears
to
be a male tactic of blocking the pregnancy by a previous
male and bringing the female quickly into
oestrous. Finally
the ‘Vandenburgh
effect’ [20]
notes that young female rats
exposed to adult males for 20 days
after weaning entered
puberty earlier than female pups not exposed to males. Male
pheromones stimulate
puberty, probably by releasing LH,
which stimulates follicular growth, presumably so that they
can mate
earlier. A related effect was noted in that female
mice housed alone attain puberty earlier than female
mice
housed together, females can thus delay puberty in
their
conspecifics, probably by
suppressing LH and FSH release
from the anterior pituitary
gland.
1.6. Pheromones and human reproductive
behaviours
Several authors have speculated that pheromones
may
influence human sociosexual
behaviours (e.g.
[21,22])
and
evidence for the effects of putative pheromones on human
sexual behaviours has come from several
sources:
1. Human correlates of animal effects
McClintock
[23] reported
that human female college
students demonstrated synchrony in their menstrual
cycles when housed in shared
accommodation (Lee–Boot
effect).
Preti et al. [24]
extended this research by applying
extracts of female sweat to the
upper lips of female
volunteers three times per week for 4 months. At the end
of this time the participants
showed significantly
greater
menstrual synchrony than volunteers in a control group.
Cutler et al.
[25] also
showed that the application of male
axillary secretions to the upper lips of female volunteers
also had a
regulatory effect on the menstrual cycle
(Whitten effect). Ellis and Garber
[26] showed
that girls
in stepfather-present homes experienced faster puberty
than girls in single-mother homes, the
younger the
daughter when the new male arrived on the scene then the
earlier her pubertal maturation
(Vandenburgh effect).
2. Laboratory studies
In an early report, Kirk-Smith et al.
[27] asked 12
male
and female undergraduates to rate photographs of people,
animals and buildings using 159-point bipolar
scales
(e.g.
unattractive–attractive),
while wearing surgical masks
either impregnated with androstenol or left undoctored.
Mood ratings were also
completed. In the presence of
androstenol, male and female stimuli were also rated as
being
‘warmer
’ and
‘more
friendly’. Van Toller et al.
[28]
showed that skin conductance in volunteers exposed to
androstenone was higher than that of
non-exposed
volunteers thereby providing evidence as to the
physiological effects of pheromone exposure.
However,
Benton and Wastell [29]
had groups of females read
either a neutral or a sexually arousing
passage whilst
exposed to either androstenol or a placebo substance.
While sexual arousal was higher in the
‘arousal’
condition, the authors found no evidence that
exposure
to androstenol had
influenced sexual
feelings.
Filsinger et al. [30]
asked males and females to rate
vignettes of a
fictional target male and female
using
semantic differentials, and also to provide a selfassessment
of mood. The test materials had been
sealed
into plastic bags, which were either impregnated with
androstenol, androstenone, a synthetic musk
control, and
a no-odour control. Females exposed to androstenone
produced lower sexual attractiveness ratings
of the target
male, while males exposed to androstenol perceived the
male targets to be more sexually
attractive.
The interpretation from such studies is further
complicated by two factors. Firstly, female
olfactory
sensitivity is moderated by the menstrual cycle with
smell sensitivity peaking at ovulation
[31]. Benton
[32]
reported that androstenol application
influenced ratings
of subjective
mood at ovulation, and Grammer [21]
found
that females rated androstenone differently at
various
phases of their menstrual cycle. Secondly, the use of oral
contraception may affect smell sensitivity
and gonadal
hormone levels thereby possibly disrupting pheromone
detection. Use of the contraceptive pill does
indeed
appear to influence female
perception of
androstenone
[21].
More recently Thorne et al. [33]
employed a repeatedmeasures,
double blind, balanced crossover
design to
assess the possible
influence of menstrual cycle
phase
K. Grammer et al. / European Journal of Obstetrics &
Gynecology and Reproductive Biology 118 (2005)
135–142
137
and contraceptive
pill use. Sixteen pill and non-pill users
were tested during both menses and mid-cycle in
both
pheromone-present and pheromone-absent conditions.
During each session (four in all) the volunteers rated
male
vignette characters, and photographs of male faces, on
various aspects of attractiveness. Pheromone
exposure
resulted in significantly
higher attractiveness ratings of
vignette characters, and faces. Use of the contraceptive
pill or menstrual
cycle phase had equivocal effects on
some vignette items but neither had any
influence on
female ratings of male
facial attractiveness.
Not all laboratory studies have found positive results
however (e.g.
[34]), and some
authors are sceptical that
higher primate reproductive behaviours are
significantly
influenced by pheromones
[35]. Thus,
while the current
scientific
opinion regarding the existence of human
pheromones remains positive, opinion remains divided as
to whether
such substances do in fact influence
human
sociosexual behaviours. This is probably due to the fact
that while a wealth of laboratory-based studies
has been
conducted, very different methodologies mean that
comparisons between studies are
difficult.
Furthermore,
methodologically solid double blind, placebo-controlled,
crossover studies are few and far
between, the Thorne et
al. [33]
study being an exception. However, that study
was laboratory based
and simply required participants to
rate the attractiveness of hypothetical opposite-sex
characters based on
written descriptions and photographs.
The ecological validity of such laboratory-based
studies is therefore
questionable.
3. Real-life studies
While laboratory studies are able to exert more control
over the varying
factors involved, of potential greater
relevance are studies assessing the effects of pheromones
in real-life
situations. Early studies were, however, not
promising. For example, Morris and Udry
[36]
prepared
aliphatic acid smears, formulated to mimic
concentrations
shown to be effective in enhancing monkey
reproductive behaviour. The solution was smeared
on
the chests of 62 married women on eight randomly
assigned nights through three menstrual cycles.
Volunteers
did not report any increase in sexual intercourse on
these test nights. However, Cowley and
Brooksbank
[37]
asked males and females to wear a necklace either
containing an opposite-sex pheromone or a
control
substance while they slept. The next day, they found that
women who had worn the male pheromones in
their
necklace reported
significantly more interactions
with
males than the control group.
Two studies which have often been cited as the
strongest evidence yet
provided for the influence
of
pheromones on human sociosexual behaviour are those
of Cutler et al.
[38] and McCoy
and Pitino
[39].
Both
studies employed double blind, placebo-controlled
methods and focussed upon the effects of
synthetic
pheromones on self-reported sociosexual behaviours in
young men
[38] and women
[39]. In the
first study
[38] 38
male
volunteers recorded the occurrence of six sociosexual
behaviours (petting/affection/kissing; formal
dates;
informal dates; sleeping next to a partner; sexual
intercourse; and masturbation) over a 2-week
‘baseline’
period. Over the next 6 weeks the volunteers kept
the
same records while daily applying a male pheromone or a
control substance added to their usual aftershave
lotion.
The authors reported that a
significantly higher proportion
of
pheromone users compared to placebo users
showed an increase from baseline in
‘sexual
intercourse’
and
‘sleeping next to a romantic
partner’. In general 58%
of the
pheromone group compared to 19% of the placebo
group showed increases in two or more behaviours
compared to
baseline; 41% of the pheromone group
compared to 9.5% of the placebo group showed increases
in three or more
behaviours compared to baseline.
In the second study [39]
36 female volunteers recorded
the occurrence of the same six
socio-sexual behaviours and
an additional behaviour
‘male
approaches’ over a
2-week
‘baseline[/size
]’ period. Over the next 6 weeks they then
either
applied a synthetic female pheromone or a control
substance added to their usual perfume on a daily
basis.
While the groups did not differ in their sociosexual
behaviours at baseline, a
significantly higher proportion
of
the pheromone group showed increases in the following
behaviours:
‘sexual
intercourse’,
‘sleeping next to
a
partner’,
‘formal
dates’ and
‘[font=AdvP41153C]petting/affection/kissing[/fon
t]’.
However, as pheromone exposure can shift the
timing of
ovulation, the authors recalculated the data to only include
the
first experimental cycle. After these
recalculations the
pheromone group only
significantly differed from
the
placebo group in ‘sexual
intercourse’ and
‘formal
dating’.
In terms of percentages,
three or more sociosexual
behaviours increased over baseline in 74% of pheromone
users but only 23% of placebo
users. As there was no
increase in self-reported masturbation the authors argued
that the changes did not
reflect changes in
sexual
motivation, but that the pheromones had
‘‘positive sexual
attractant
effects. . .’’
(p. 374).
The results of these studies appear to provide
impressive
evidence for the effects of synthetic pheromones
on sexual attractiveness. However, there are a
number of
methodological problems with the studies,
which make the
findings less emphatic. Firstly,
the
studies did not control for the attractiveness of the
volunteers nor make allowance for this when
allocating
the conditions. If for example the pheromone groups had
contained slightly more attractive
individuals than the
control groups, then subsequent positive effects attributed
to pheromones may be
misleading. Secondly, all the
data were of the self-report kind (prone to error and
subjective bias especially
as
‘back[s
ize=2]filling’
was allowed in
the second study) and as such no objective record of
the
putative effects of pheromone versus placebo were
obtained. Thirdly the groups differed widely in terms
of
K. Grammer 138
et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology
118 (2005)
135–142
their dating status with some being married, some in
long-term relationships and others
being single. Those in
relationships would have certainly recorded more of
certain sociosexual behaviours than
the single volunteers,
it would have been better if the entire subject pool were
single males seeking more
dating/sex opportunities.
Fourthly, the baseline period of 2 weeks is
difficult to
equate with a testing
period of 6 weeks even though
average differences from baseline were analysed. How
can we be sure that the
social behaviour of the volunteers
changed not as a result of pheromone exposure but by
other factors during
the experimental period, e.g. going
on holiday, celebrating at an
office party? While the
actual
behaviours were recorded, the context within
which those behaviours occurred was not controlled for.
The
evidence from these two studies thus indicates
that certain sociosexual behaviours are increased in
males and
females who wear pheromones, compared to
baseline. However, the studies do not convincingly show
that the
pheromone and placebo groups were well
matched; that the baseline and experimental conditions
were matched in
terms of various temporal and
behavioural factors; that objective changes in sociosexual
behaviours did occur;
and that the pheromones served as
a
‘sexual
attractants’ rather than say a mood
enhancer,
confidence builder,
etc.
4. Genetic signalling
Various
‘good
genes’ theories of sexual selection
have
emphasised the importance of
immunocompetence
[40,41]
in that females can obtain good genes for their
offspring by
mating with males whose genes are
complementary to their own. A possible mechanism
by which this can be
achieved is via body odour. The
major histocompatibility complex (MHC) is a large
chromosomal region
containing closely linked polymorphic
genes that play a role in immunological self/
non-self recognition; this
genetic information is relayed
by androgen-based pheromones
[42]. Numerous
studies
in rodents have now established that MHC genotype is
involved in odour production, and such odours are
used in
individual discrimination
[43]. House
mice learn the
MHC identity of their family during development and
avoid mating with individuals carrying
familial MHC
genes; they do so through the use of odour cues from
urine (e.g.
[44,45]). Is
there any evidence that humans
possess these abilities?
Some studies have shown that women seem to
prefer
the odours of immunocompatible men. Wedekind et
al.
[46]
HLA-typed (Human Leukocyte Antigen is the
human MHC) 49 women and
44 men and asked the
women to rate the attractiveness of the odours of t-shirts
worn by three MHC-similar and
three MHC-dissimilar
men.Women rated the odour of the MHC-dissimilar men
as
‘more
pleasant’, and this odour was
significantly more
likely to remind
them of their own mate’s
odour.
Interestingly, the preferences of women taking an oral
contraceptive were
reversed—they preferred the
MHCsimilar
odours. This could be due to the fact that oral
contraceptives mimic the effects of pregnancy,
and
pregnant females may be attracted to MHC-similar
individuals who are likely to be close kin and
potential
reproductive helpers.
In a similar study, Thornhill and Gangstad
[47]
measured bilateral physical traits in males and females
and then asked the volunteers to wear the same
T-shirt for
two consecutive nights. Opposite-sex participants then
rated the shirts for
‘pleasantness’,
‘sexiness’
and
‘[fo
nt=AdvP41153C]intensity’;
donor’s facial attractiveness was
also
assessed by different opposite-sex volunteers. Non-pill
users in the fertile phase of their menstrual
cycle gave the
T-shirts worn by symmetrical males higher ratings; this
was not seen in females using the
contraceptive pill, or in
females at unfertile phases of their cycle. Female
symmetry had no
influence on male ratings. The
authors
proposed that the so-called
‘scent of
symmetry’ is an
honest indicator of
male genetic quality.
In a real-life study of actual mate choices, Ober et
al.
[48]
found evidence for HLA-dependent mate preferences
in a population
of Hutterites (a small, genetically
isolated religious sect). They found that couples were less
likely to
share MHC haplotypes than chance, and in
couples that had a similar MHC they demonstrated
unusually long
inter-birth intervals (unconscious avoidance
of inbreeding?).
Milinski and Wedekind
[49] HLA-typed
males and
females and then asked them to smell 36 scents
commonly used in perfume/aftershave. They rated
each
scent on whether they liked it or not, and whether they
would use it on themselves. The authors reported
a
significant correlation between
HLA and scent scoring
for themselves but not for others, showing the people
unconsciously select perfumes to
enhance their own body
odours that reveal their genetic
make-up.
1.7. Pheromones and the battle of the
sexes
Differential parental investment theory
[50] predicts
that
when looking for long-term relationships females should
seek out and choose males who are ready to invest
resources
in their offspring. This minimizes female investment, but
maximizes overall investment through added
male assistance.
In contrast, males are expected either to attempt
copulation frequently and with as many
fertile females as
possible, or to develop a long-term pair bond. This helps to
ensure that either a large
number of offspring survive
without
significant paternal investment, or
that male parental
investment occurs primarily when another male does not
father offspring.
According to
this theory, it is adaptive for females and
males to develop and use cognition in mate selection, which
takes
into account biological constraints. Thus, mate
selection is a task of information processing, and
evolution
K. Grammer et al. / European Journal of Obstetrics
& Gynecology and Reproductive Biology 118 (2005)
135–142
139
would have
favoured individuals who were able to quickly
and reliably process information that allowed them to
make
appropriate mating decisions. Adaptive cognition could be
expected to lead to optimal decision-making
under a wide
spectrum of socio-economic constraints. The existence of
ubiquitous sex
specific differences in mate selection
criteria
[51]
attests that male and female cognition is adapted to
the
biological constraints of mate selection.
Neither males nor females can perceive ovulation in
humans
consciously. This is surprising in the light of the fact
that it has been shown to be associated with a number
of
overt physiological and behavioural changes. One
‘unconscious’
mechanism associated with these menstrual
cycle
changes might be that of olfactory perceptions.
Alexander and Noonan
[52], and
Symons [53]
have
argued that hidden oestrous has evolved because
females
need to trick males into forming a bond. Males unaware
of
female’ s fertility would remain
bonded to ensure
impregnation and paternity. A female providing clues to
her ovulation might risk losing male
investment, due to
paternal uncertainty and the limited temporal reproductive
interaction. This development
would implicate the male fear
of cuckoldry as an evolutionary pressure
[50]. The
outcome
would be that the female’s
ability to secure paternal care is
affected by mechanisms that increase temporal aspects of
the pair bond and
enhance male confidence of
paternity.
In contrast with this line of argument, Benshoff and
Thornhill
[54] and Symons
[53] have
proposed a second
evolutionary scenario in which hidden oestrous evolved to
increase the chances of successful
cuckoldry by females so
they ‘‘can
escape the negative consequences of being pawns
in marriage games’’
([55]
p. 350). Once monogamy is
established, a
female’s best strategy would be to
copulate
outside the pair bond because she can then obtain superior
genes with a certain expectation of
paternal investment. In
this case the outcome is genetically superior offspring.
These two hypotheses imply
different impacts of
heritable traits. If those genes which induce paternal care
were relevant for offspring
success, a male paternitysecuring
function for lost oestrous would be possible. If
there are other relevant
traits not related to paternal care but
relevant to offspring survival, then hidden oestrous could
allow
females to exploit occasional opportunities to mate
outside the pair bond
[56]. In both
cases, male knowledge of
ovulation may be selected against because it would hinder
the
female’s mating strategies
[52,57].
Rec
ently, the second hypothesis has received considerable
support. Bellis and Baker
[58] conducted
a study of
2708 females and found those 13.8% of 145
‘unprotected’
extra-pair copulations (EPC) occurred during
the fertile
period and were preceded in most cases by intra-pair
copulations (IPC). EPCs were rarely followed
by IPCs.
According to his study EPC and thus female
infidelity peaks
at ovulation. The
authors conclude that these results hint at
female-induced sperm competition, which would be
expected by the
second hypothesis of the evolutionary
function of concealed ovulation discussed above. Still it is
unclear
what proximate mechanism or mechanisms cue
female EPC at ovulation. The assumption that concealed
ovulation
serves to deceive males is common to all these
theories. Supposedly, females deceive males about the
fertile
phase of the menstrual cycle to help ensure male parental
investment, which yields an optimal number
of offspring.
Additionally, concealed ovulation helps females to monopolize
reproduction and, as a
consequence, forces males to
develop reproductive strategies for gaining access to
ovulating females. It is
reasonable to expect male counter
strategies would develop against the deceptive attempt by
females to conceal
ovulation. Grammer [21]
described a
possible male counter strategy: the evolution of
the
androstenone–androstenol
signalling system. In his study,
290 female subjects rated the odour of androstenone. A
change in assessment
throughout the menstrual cycle was
found: at the time of ovulation the women found the scent of
androstenone,
the most dominant odour of the male armpit,
to be more pleasant than on the other days of the menstrual
cycle.
These results suggest that there is a change in the
emotional evaluation of males triggered by the reaction
to
androstenone. The findings
support previous results by
Maiworm
[59], which
were of borderline significance.
Male
body odour is usually perceived as unattractive and
unpleasant by females but this evaluation changes at
the
point in the menstrual cycle when conception is most likely.
This
finding is underlined by the fact that
anosmia to
androstenone also varies with cycle. At the conceptual
optimum we
find fewer anosmic females. It could
be
suggested that changes in anosmia during the cycle could
also be a female strategy, although more data need
to be
gathered to prove this hypothesis. Thus the change in female
attitudes towards male body odour could
have a strong
impact on mate selection and perhaps self-initiated
copulations by females. If we regard the
androstenol–
androsten
one-signaling system, the situation for androstenol
seems clear, it makes males more attractive for
females.
Female advantage in this case is nil, unless
fitter males
produce more
androstenol. The situation is more complicated
because producing androstenol inevitably produces
androstenone.
The androstenone production has a disadvantage
in its unpleasantness. Hence
attractiveness-enhancing
androstenol immediately oxidizes to androstenone,
which repels females. A
non-producing male could do quite
well in a population of producers, because females would
not be repelled by
his body odour. So the attractivenessenhancing
component of the smell does not seem to be the
main, or at
least only, function of the signalling system.
Regarding androstenone, the fact that females assessed
its
odour as more pleasant at the time of ovulation could be of
advantage for males, as odorous males will be
more
successful when approaching ovulating females, rather than
non-ovulating females. This suggests that
males use a kind
of passive
‘ovulation-radar’ for the detection of the actually
hidden
ovulation.
K. Grammer
140 et al. / European Journal of
Obstetrics & Gynecology and Reproductive Biology 118 (2005)
135–142
Females faced with an evolved male strategy to detect
hidden ovulation would be likely
to develop a counter
strategy. One possible strategy could be to manipulate male
cognition and thus adaptive
male information processing in
mate selection. Research on many species of non-human
primates (especially on
rhesus monkeys) has shown the
ability to perceive ovulation by smell. Although normally
motivated to copulate,
when sexually inexperienced rhesus
males were made anosmic they showed no further sexual
motivation despite a
powerful visual cue: the
female’s
swelling
[60].
Furthermore, rhesus males show no interest in
ovariectomized rhesus females, presumably because
ovariectomized
rhesus females lose the odour characteristic of
ovulation. Rhesus males regain interest in
copulation when
the vaginal secretions from non-ovariectomized females are
applied to ovariectomized females.
Studies on menstrual
cycle
fluctuations in the fatty-acid
composition of women’s
vaginal
fluids indicated that a similar type
of signalling
system might also exist in humans [16,
61–[col
or=#000066]63][/color]. For example,
human vaginal secretions have a
composition that is similar
to the vaginal secretions of female rhesus monkeys. The
application to
ovariectomized female rhesus monkeys, either
of human, or rhesus vaginal secretions, induced
similar
activation of rhesus male sexual interest
[64].
The
behaviourally active fraction of the rhesus
vaginal
secretions—referred to as
‘Copulins’—consists of volatile,
short-chained fatty acids
[65]. These
same substances (i.e.,
the short-chained fatty acids: acetic, propanoic, butanoic,
methylpropanoic,
methylbutanoic, methylpentanoic acid)
occur in human vaginal secretions, albeit in slightly different
amounts
[16]. In
addition, the composition of these copulins
varies during the menstrual cycle
[62].
Cowley
et al. [66]
found that rhesus vaginal secretions
change
peoples’ assessment of other people,
and that the
application of copulins tends to yield a more positive
impression of females. Doty et al.
[67] used a
questionnaire
to evaluate the intensity and pleasantness of different
vaginal
fluids from a
complete menstrual cycle. They found that
odour at ovulation was both the most intense odour and the
least
unpleasant.
In a study by Juette (unpublished data) synthesized
female vaginal secretions
(‘Copulins’) were tested for their
ability to act as signals for males.
Menstrual, ovulatory and
pre-menstrual fatty acid compositions of Copulins and an
odourless water control were
presented to 60 non-smoking
male subjects for 25 min in a double-blind experiment. To
control for changes in
sex hormones that were induced by
copulins, saliva-samples were taken before and after presentation.
While
inhaling either a composition of copulins or a
control, males rated pictures of females for attractiveness.
It
was shown that ovulatory fatty acid compositions stimulated
male androgen secretion and changed the
discriminatory
cognitive capacities of males with regard to female attractiveness
in that males became less
discriminating. As we can
learn from the above examples, human pheromones seem to
work as beautifully balanced
‘strategic
weapons’ in
the
‘battle of the
sexes’ and the
‘war of
signals’ resulting from
asymmetric
investment theory.
2.
Conclusion
As we can learn from the reviewed studies
on
pheromones, the model of humans being only optical
animals has to be revised. Human sociosexual
interactions
are influenced by
pheromones, even if they cannot be
detected consciously. Pheromones have the potential
to
influence human behaviour and
physiology and so there has
to be asked the question, in which way the modern striving
for cleanliness and
odourlessness affects our everyday social
lives and human reproductive success in the future. What we
know at
the moment, as many studies in the last few years
have pointed out, is that the human sense of smell has by
far
been underestimated in the past and that humans, like other
animals, use olfactory signals for the
transmission of
biologically relevant
information.
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