Human pheromones and sexual attraction from medical journal 2004

[Dr.Mercury]

Review

Human pheromones and

sexual attraction

Karl

Grammer

a,

Bernhard

Finka[font=AdvP41153C],[/

font]*, Nick

Neaveb

a

Ludwig–Boltzmann-Institute for Urban Ethology, c/o

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

Austria

b

H

uman 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

[/font

]

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

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

–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

[fon

t=AdvP41153C]–

12][/size

]. Recently, the

identification of a pheromone




receptor gene expressed in human olfactory mucosa has

further strengthened the case for a functioning VNO

[13].



Further 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]).

[/left

]

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]’

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–[font=AdvP4B2E3F]142

[

/font]

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-Boo

t 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

[font=AdvP41153C]

[21]

[/fo

nt].


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



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

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’

[left

]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

‘

base

line’ 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]fi[/size]lling’

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–[font=AdvP4B2E3F]142

[

/font]

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

‘

intensity’[siz

e=2]; donor[/size]’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].



Recently, 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–

[left

]androstenone-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.

[/left]

K. Grammer

140 et al. / European Journal of

Obstetrics & Gynecology and Reproductive Biology 118 (2005)

135–[font=AdvP4B2E3F]142

[

/font]

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

ui

ds 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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