Review
Human pheromones and sexual

attraction
Karl

Grammer
a,

Bernhard

Finka,[/

font]*, Nick

Neaveb

[size=

1]
a[/size]
Ludwig–Boltzmann-Institute for Urban Ethology, c/o Institute of

Anthropology, University of Vienna, Althanstrasse 14, A-1090 Vienna,

Austria

b
Human

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
[size=

1]
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.
[/size]
#
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

in
fluence 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

identi
fication 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

in
fluence 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

in
fluenced 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

in
fluenced 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 signi
ficantly

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

in[font

=AdvP41153C]fl
uenced 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

signi
ficantly 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

signi
ficantly 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

‘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

dif
ficult 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

speci
fic 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

in
fidelity 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

fl
uids 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 in
fluenced 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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