Human
Pheromones:
"Integrating Neuroendocrinology and Ethology"
by James V. Kohl*,
Michaela Atzmueller, Bernhard Fink & Karl Grammer
*JVK Resources, Inc. Las Vegas, Nevada, USA.
Ludwig-Boltzmann-Institute for Urban Ethology, University
of Vienna, Vienna, Austria.
Keywords:
human ethology, pheromones, odor, olfaction,
human sexuality, sexual selection, mate choice
Submitted:
August 6, 2001
Accepted: September 10, 2001
Abstract:
The
effect of sensory input on hormones is essential to any explanation
of mammalian behavior, including aspects of physical attraction.
The chemical signals we send have direct and developmental effects
on hormone levels in other people. Since we don't know either
if, or how, visual cues might have direct and developmental
effects on hormone levels in other people, the biological basis
for the development of visually perceived human physical attraction
is currently somewhat questionable. In contrast, the biological
basis for the development of physical attraction based on chemical
signals is well detailed.
The
human sense of smell
The
importance of the human sense of smell has been largely underestimated.
Many people believe that human olfactory acuity and specificity
have deteriorated. Other mammals are believed to be macrosmatic
(i.e., better smellers) because they have more olfactory receptor
cells in their nasal mucosa than humans [1].
For example, dogs have about 230 million olfactory receptor
cells, while humans have about 10 million. Accordingly, humans
and other primates typically are believed to be microsmatic
(i.e., worse smellers) equipped with highly developed powers
of vision that supposedly make humans "visual creatures."
This concept needs reconsideration since many recent studies
have shown that olfaction plays a very important role in human
reproductive biology and because human reproductive biology
affects human behavior.
The nasal mucosa can functionally be divided into two areas:
the respiratory region and the olfactory region, which contains
the sensory cells. In the nose, the olfactory region can be
found on both sides of the nasal septum in the upper nasal conchae.
The ability to discern between many different odors suggests
that specific receptors exist in the sensory cells. Excitation
of axons from these sensory cells occurs when an odor molecule
"docks" with a receptor protein in the membrane of
the olfactory ciliae. It is not yet known whether the human
ability to distinguish between thousands of different scents
is caused by the number of specific receptors or by the simultaneous
stimulation of multiple receptors [2, 3].
It is suspected, however, that our superior cognitive power
allows us to better use olfactory input when compared with other
mammals [4]. The axons of the sensory cells
enter the olfactory bulb. Sensory input is then projected via
the olfactory tract into the olfactory lobe of the brain. From
here, olfactory input is projected via the thalamus to the neocortex
and to the limbic system. This pathway allows olfactory stimuli
to be consciously detected and interpreted, but also allows
olfactory stimuli to directly influence the neuroendocrinology
of emotions.
The affective primacy hypothesis' [5]
asserts that positive and negative affective reactions can be
evoked with minimal stimulus input and virtually no cognitive
processing. Olfactory signals seem to induce emotional reactions
whether or not a chemical stimulus is consciously perceived.
We theorize that the importance of human non-verbal signals
is based upon information processing, which occurs in the limbic
system, and without any cognitive (cortical) assessment. Affect
thus does not require conscious interpretation of signal content.
Underlying this fact is that affect dominates social interaction
and it is the major currency in social interactions [6].
Affective reactions can occur without extensive perceptual and
cognitive encoding. They are made with greater confidence than
cognitive judgments, and can be made sooner [5,
7]. Olfactory input from the social environment
is well adapted to fit such assertions. For example, chemical
cues allow humans to select for, and to mate for, traits of
reproductive fitness that cannot be assessed simply from visual
cues.
The universal nature of emotional expression in different species
strongly suggests the shared evolution and the fundamental nature
of affect. Affect is clearly primary to language in phylogeny.
Affect comes before our evolved language and our present form
of thinking. Many studies have shown that the contribution of
affect to signal recognition and processing has been underestimated
[8, 9, 10].
Despite agreement that the affect-cognition question is important
to research in non-verbal behavior, there are still many questions
that current data do not answer.
In contrast, the affect of pheromones on our emotions is linked
to the effect of pheromones on the hormones of the hypothalamic-pituitary-gonadal
axis - an unconscious affect. The ontogenetic link between olfaction
and hormones becomes evident in patients suffering from X-linked
Kallmann's syndrome. They show underdeveloped gonads, completely
lacking secondary sexual characteristics, and both male and
female patients are anosmic, which means they are unable to
detect odors. This syndrome results from underdevelopment of
the olfactory bulb in the embryo. Gonadotropin releasing hormone
(GnRH) neurosecretory cells of the hypothalamus originate in
the olfactory placode and migrate into the hypothalamus. However,
in Kallmann's syndrome this migration does not occurand this
is accompanied by underdevelopment of the olfactory bulb and
minimal, if any, secretion of hypothalamic GnRH [11].
Preliminary evidence suggests that people with Kallmann's syndrome
do not respond to putative human pheromones [12].
Further to our discourse on affect, which includes the effect
of human pheromones on hormones like GnRH, and thus on behavior,
is the concept that affect is conditioned in the presence of
other sensory input. For example, Cooper, Parvopassu, Herbin,
and Magnin [13] suggest that mammalian neuroanatomical
pathways link vision and olfaction. Socialenvironmental odor
cues, which male rats may learn to visually associate with sexual
activity, can be used to condition luteinizing hormone (LH)
release [14]. In fact, after minimal conditioning,
an arbitrary odor ultimately will elicit a male LH response,
even in the absence of odor previously associated with a female.
Regardless of whatever non-olfactory sensory input is involved,
the functional significance of the conditioned change in LH
secretion lies principally in the unequivocal demonstration
that olfactory cues can activate the male pituitary-gonadal
axis in a way that mimics, in every respect, the activation
achieved by exposure to a female. Short-term exposure of males
to females also is linked to increased testosterone (T) in rats,
mice, rabbits, bulls, rams, monkeys, and humans [14].
From a neuroendocrine perspective, given the link between LH
and T, presumably, the female odor cues that condition LH release,
also condition T release, and therefore have the ability to
condition human hormone responses to non-olfactory sensory input.
This biologically based affective reaction links the social
environment to the neuroendocrinology of behavior, and does
not require cognition. Based upon a detailed mammalian neuroendocrine
model, Kohl [15] proposed that LH is the measurable
link between sex and the human sense of smell. Kohl [16]
detailed reciprocity in olfactory-genetic-neuronal-hormonal-behavioral
relationships that appear to link the nature and nurture of
human sexuality. Subsequently, Diamond, Binstock, and Kohl [17]
offered a more complete overview of nongonadal, nonhormonal,
influences on sexual differentiation and of the influence of
sensory stimuli, especially chemosensory stimuli, on human sexuality.
In this regard, the affect of chemosensory stimuli on behavior
was integrated with tactile cues. Dellovade et al. [18]
suggest that male pheromones and tactile cues lead to the increase
they noted in GnRH immunoreactive (GnRN-ir) cell numbers which
were correlated with LH modulated estradiol levels and with
sexual behavior.
Pairing of a neutral odor with access to a receptive female
rat was shown to result in an ejaculatory preference for a female
with that odor [19]. Plaud and Martini [20]
recently found that the sexual arousal of human males could
be classically conditioned. This was confirmed by Lalumiere
& Quinsey [21] who showed that sexual
interest in human males might result from Pavlovian conditioning.
It seems likely that odorinduced, GnRHdirected conditioning
of human LH release may be used to evoke functional changes
in the mammalian neuroendocrine pathways that mediate the release
of T and E, with or without visual awareness of any associated
stimuli. Given mammalian models, olfactory conditioning of a
GnRH-directed neuroendocrine response may lead to a change in
the sex steroid hormones T and E, which would be a change that
also is manifest in behavior. This neuroendocrine link between
social environmental sensory (i.e., olfactory) input and the
neuroendocrinology of reproduction appears to preclude any involvement
of cognition. Thus, the affect-cognition question is sublimated
by the effect of pheromones on the neuroendocrine system, and
presumably on behavior. For example, though neuroendocrine effects
were not measured, Jacob, Kinnunen, Metz, Cooper, and McClintock
[22] showed through brain imaging that androstadienone
has distributed effects on cortical processes and brain metabolism
even when it is not detected consciously. Accordingly, this
human "chemosignal" modulates psychological state
without being consciously discernible as an odor (see also [23]).
The
vomeronasal organ
The
vomeronasal organ (VNO), also termed Jacobson's organ, is a
special part of the olfactory system(s) and can be found in
most tetrapods at least in the embryonic stages. In most mammals,
it is located above the hard palate on both sides of the nasal
septum and consists of a pair of blind-ended tubes that open
into the nasal cavity. In some mammals, it is connected to the
oral cavity by the nasopalatine duct. Receptor cells in the
epithelium of the mammalian VNO are not equipped with cilia
[24, 25, 26]
and their axons extend to an "accessory" olfactory
bulb, that projects directly into the limbic system, bypassing
the thalamus, and thus cortical integration. Simply put, the
VNO is representative of an accessory olfactory system [27]
that directly translates olfactory cues into neuroendocrine
responses. In the past, the VNO was believed to exist only in
lower mammals, and only at embryonic stages in primates. However,
recent data have shown that the VNO also exists in adult humans
[28]. Monti-Bloch and Grosser [29]
found the adult human VNO responds to picogram amounts of human
skin pheromones with depolarization. These findings suggest,
that the human VNO may function as a pheromone detector as it
does in other mammals. However, so far there is no evidence
that the human VNO is connected to a functional accessory olfactory
system. This lack of evidence, in the past, has caused considerable
scientific debate about whether or not there is such a thing
as a human pheromone.
Pheromones
The
term "pheromone" comes from the ancient Greek words
"pherein": to carry, and "hormon": to excite.
Karlson and Luscher [30] introduced this term
in 1959. Pheromones are referred to as ecto-hormones: chemical
messengers that are transported outside the body that have the
potential to evoke certain responses, such as physiological
(e.g., hormonal) or behavioral changes in a conspecific. Thus,
pheromones play an important role in inter-individual communication,
and are known to do so in species from single-celled yeasts
to primates, despite different manifestations of what might
be considered "behavior".
Pheromones can be divided into at least two classes, according
to the physiological effects they cause in the recipient: "signal"
and "primer" pheromones [31]. Signal
pheromones cause short-term changes, such as the release of
neurotransmitters that can directly modify the recipient's behavior.
For example, Moss and Dudley [32] suggest
that a fraction of the GnRH molecule functions directly as a
neurotransmitter in rats to elicit a behavioral effect (i.e.,
lordosis). This behavioral effect is characteristic of a "signal"
pheromone, which activates a response.
Primer pheromones evoke long lasting changes in the body by
influencing the hypothalamic-pituitary-gonadal axis, which allows
both for organizational and activational effects of primer pheromones.
Primer pheromones are believed to exert their affect by altering
the hypothalamic secretion of GnRH. Hypothalamic GnRH triggers
the secretion of gonadotrophic hormones from the pituitary.
The gonadotropins follicle stimulating hormone (FSH), and LH
affect gonadal hormone secretion. In females, FSH stimulates
follicle maturation in the ovaries and the secretion of estrogens;
LH stimulates the ovarian theca cells to produce androgens,
which diffuse to the granulosa cells of the ovarian follicle,
where they are converted to estrogens, and LH also stimulates
the growth of the corpus luteum and secretion of progesterone.
In males, FSH stimulates spermatogenesis and probably affects
T production and secretion by acting indirectly on an asyetunidentified
Sertoli cell protein [33]. In males, the LH/FSH
ratio controls T production by Leydig cells in the testes. Sex
steroid hormones like T and E alter neurotransmission by influencing
synaptogenesis, synaptolysis, and apoptosis during development.
GnRH pulsatility is unequivocally required for LH release (see
[34]), and GnRH pulsatility is directly associated
with changes in LH and in FSH pulsatility that are manifest
in LH/FSH ratios, which modulate steroidogenesis. Thus, LH and
the LH/FSH ratio are human measures of GnRH pulsatility and
so are T and E levels, though these measures are less direct.
The effect of primer pheromones on GnRH allows pheromones to
influence LH/FSH ratios and the production of T and E, or simply
put, primer pheromones influence the entire hypothalamic-pituitary-gonadal
axis, which influences behavior by altering neuroanatomy and
thus neurotransmission.
The odors produced by humans are a function of the location
on the body where the odor is being produced. The amount of
available oxygen as well as water and skin gland secretions
determine the type and number of cutaneous flora, which are
present on different body areas. Moist areas of the body, such
as the mouth, axillae, genital region, and feet, support greater
varieties and numbers of bacteria because they are occluded,
or are moist because of their function (e.g., mouth, vaginal
barrel). The type and density of cutaneous microorganisms on
different areas of the body interacting with skin and other
glandular secretions give rise to a variety of odors from various
body sites.
Human
body odor
In
humans, pheromone production is primarily linked to the apocrine
glands of the skin, but also is linked to other glandular secretions
and to skin flora present in moist areas of the body, like the
axillae, mouth, feet, and genitals. For example, concentrations
of C2-C5 aliphatic acids that are secreted from the vaginal
barrel, and that have been referred to as "copulins,"
vary with menstrual cycle phase. The odor of the copulins and
its behavioral effects also appear to vary with the menstrual
cycle. Thus, copulins are also referred to as pheromones [35,
36].
In sufficient quantity, pheromones are consciously detected
as natural human body odor. Apocrine glands are found in areas
that include the genital area, around the navel, on the chest,
breasts, and areola, and are concentrated in the axillae. Like
ecrine (watery sweat) glands and sebaceous (sebum-secreting)
glands, apocrine glands are associated with hairs. The high
concentration of apocrine glands found in the armpits led to
the term: "axillary organ", which is considered an
independent "organ" of human odor production. Apocrine
glands have a tubular, coiled structure and are about 2 mm in
diameter [37]. Human apocrine glands develop
in the embryo, but become functional only with the onset of
puberty [38]. This link between apocrine gland
function and puberty reflects that function is closely linked
to levels of sex steroid hormones that increase with the onset
of adrenarche and puberty. Freshly produced apocrine secretion
has no odor [39], and is transformed into
odorous products by microorganisms (see [40]
for review).
For reasons that remain unclear, humans produce a relatively
high amount of odor production, when compared to other primates.
The odors of the skin, the saliva, urine and, genital secretions,
contribute to the amount and hedonic quality that is characteristic
of natural human body odor. In this regard, we note that any
odor, even the scent of rose, becomes aversive when it is produced
in suprathreshold quantities. Thus, though pheromonal communication
typically occurs without consciousness, pheromones, when produced
in high concentration, may still have both conscious and aversive
effects on others.
Human
pheromones
By
definition a human pheromone elicits changes in the physiology
and/or behavior of a conspecific. Stern and McClintock [41]
showed that the pheromones of women regulate ovulation in other
women, presumably by affecting levels of LH and FSH. Berliner,
MontiBloch, JenningsWhite and DiazSanchez [42]
suggest that a progesteronic pheromone alters LH pulsatility
in men. These studies show that human pheromones, or that a
putative human pheromone, elicit change in hormones. Similarly,
Juette [43] showed that an aqueous mixture
of five ovulatory fatty acids evoked increased saliva T levels
in men, and produced better judgments of female photos and of
female voices than in controls. Thus, both physiology (i.e.,
T levels) and behavior (i.e., judgment) were affected. The putative
human pheromone androstadione also has been shown to elicit
physiological (i.e., hormonal) and behavioral (i.e., mood) changes
[44, 23]. Shinohara, Morofushi,
Funabashi, and Kimura [45] showed that axillary
pheromones from women either in the follicular or in the ovulatory
phase of the menstrual cycle differentially modulate pulsatile
LH pulse frequency in other women, a hormonal effect. Preti,
Wysocki, Barnhart, Sonheimer and Leyden [46]
recently showed that male axillary extracts effect LH and mood
in female recipients, and suggested that the LH response may
be used to determine precisely what compound is involved in
this pheromonal effect, which is a typical mammalian female
response to pheromones from a male conspecific [14].
Minimally, human pheromones appear to alter both physiology
and behavior in other humans.
It is still unknown how many different pheromones are produced
in human axillae, but some of them have been investigated in
recent years. Most studies focused on the 16-androstenes, metabolites
of the characteristically male sexual hormones, the androgens,
which are secreted by the apocrine glands. Dorfman [47]
assumes that the 16-androstenes develop with the metabolism
of testosterone. Two of these androstenes, the alcohol 5-androst-16en-3ol
(androstenol) and the ketone 5a-androst-16en-3-one (androstenone)
have odorous characteristics that bear a similarity to the smell
of male axillae. Androstenol has a musk-like scent, while androstenone
smells urinous. It is important to note that the odors arise
only via the activity of microorganisms [48].
Among these microorganisms are the aerobic bacteria Corynebacterium
ssp., which transform the odorless precursors androstadienol
and androstadienone, into the odorous 5a-androstenone [49].
If the axillae are treated with antibacterial detergents, the
production of androstenone decreases significantly [50].
Male axillary sweat contains approximately five times more androstenone
than female sweat [51]. This sex difference
can be explained by sexually dimorphic levels of blood androgens,
and by sex differences in the colonization of microorganisms.
For example, Jackman and Noble [52] investigated
the axillary bacteria of 163 male and 122 female subjects and
were able to show that in most men the axillae were dominated
by the bacteria Corynebacteria ssp., whereas in women they found
the bacteria Micrococcaceae. Other putative human pheromones,
whether secreted primarily in the axillae, or in other areas,
can be expected to be identified upon the examination of sexually
dimorphic adrenal hormone metabolites, and with the identification
of other sexually dimorphic microorganism colonization.
Do
pheromones influence human behavior?
Pheromones
seem to play an important role in mammalian social and sexual
behavior. This suggests that the investigation of pheromone
effects in humans is warranted. An early study showed that skin
conduction in subjects exposed to androstenone was 1.5 times
higher than in the control group [53]. These
findings provided clues to the potential physiological effects
of the 16-androstenes. In a study by Cowley and Brooksbank [54]
38 men and 38 women wore a necklace with a pendant containing
androstenol during sleep. The next morning, the number of social
interactions of the subjects was assessed and it showed that
women wearing the necklace had had significantly more and more
intensive contact with men than subjects in the control group.
It was presumed that human pheromones had the potential to facilitate
inter-sex communication.
Another research team investigated the influence of odorous
substances on photo assessment [55]. Two hundred
men and women were told to rate a photo of a male person and
to rate their own mood under the influence of androstenone.
Men rated the person in the photo as "passive" and
women reported their own mood to be less "sexy". In
a follow-up study men under the influence of androstenone rated
photos of males positively, if they liked the scent of androstenone
[56]. In a similar study, male and female
subjects rated photos of people, animals, and buildings under
the influence of androstenol [57]. Subjects
wearing masks impregnated with androstenol rated the photos
of women as more attractive, more sexy, and friendlier, and
rated the photos of men warmer and friendlier than subjects
in the control groups.
The influence of human pheromones on social behavior may pale
by comparison to the influence that pheromones may have on human
reproduction. Olfactory cues are essential in animal, especially
mammalian, sexual behavior. In humans these olfactory cues are
difficult to isolate and related discussions have lead to controversy.
Nonetheless, humans are capable of discriminating between males
and females by olfactory cues alone [58].
The afore-mentioned sex differences in the composition of human
axillary secretions may be the basis for such discrimination.
Pheromones also influence the human menstrual cycle. McClintock
[59] found that female college students, who
spent significant amounts of time together showed synchrony
of their menstrual cycle, and attributed this synchrony to odors
(pheromones). A few years later this finding was bolstered by
another study [60]. Sweat samples of 5 women
with regular 29-days-cycles were taken daily. These donor samples
were applied to the upper lips of the female test subjects 3
times a week for 4 months. By the end of the test period, test
subjects menstruated significantly more often at the same time
as the donors than subjects in the control group. It became
clearer that menstrual synchrony, which also is indicative of
ovulatory synchrony, is controlled by pheromones. In a parallel
study, the influence of male odors on the menstrual cycle was
tested [61]. Odor samples of male axillary
secretions were again applied to the upper lips of female test
subjects. Those who were not sexually active had irregular menstrual
cycles at the beginning of the experiment. After 4 months the
mean cycle length was 29.5±3 days length in a majority
of the test subjects. This strongly suggested that male pheromones
have a regulatory effect on the menstrual cycle.
Many authors have speculated that both androstenone and androstenol
are male pheromones, raising the questions of whether and how
females perceive them. Filsinger, Braun and Monte [62]
showed that the application of androstenone to females led to
negative descriptions of males whereas the application of androstenol
led to a description of males as being sexually attractive.
It has been shown repeatedly that females either find the odor
of androstenol to be attractive, or that the perception of this
odor results in heightened female sexual arousal [63].
These results indicate that androstenol can induce positive,
while androstenone induces negative emotions towards males,
and suggest that androstenol may be a male pheromone that enhances
attractiveness.
Maiworm [64] found that females perceive males
positively under exposure to androstenol and negatively under
exposure to androstenone. The finding that females are emotionally
more affected by androstenone and androstenol than by control
substances like rose water, led to the hypothesis that both
androstenone and androstenol might be male pheromones. The role
of androstenol in any hypothetical signaling system is clear,
since it seems to promote female sexual attraction towards males.
However, problems arise in attempts to determine the function
of androstenone, which induces negative female emotions towards
males. Besides, androstenone is the more prominent odor. Thus,
the odor of androstenone will prevail, whereas the fresh sweat
odor of androstenol disappears quickly. The fact that the production
of attractiveness-enhancing androstenol inevitably produces
the repellent androstenone makes it difficult to propose a definite
advantage for the sender of such chemical signals compared to
a non-sender. Arguably, a pheromone function of both substances
is unlikely. If a male repels females with androstenone, this
would contradict hypotheses, which assert male promiscuity on
an evolutionary basis [65]. A less odorous
male could out reproduce a more odorous male, simply because
he could approach more females in less time and with less energy.
This only holds if the costs of the more odorous androstenone
production are greater than the benefits reached through producing
the more sexually attractive androstenol. As androstenol oxidizes
to androstenone the initial attractive signal becomes repellent.
Because this effect takes place within 20 minutes [66],
a less odorous male would be better off, since the repellent
smell of androstenone is the long-term prevailing signal. If
androstenone is a signal for females, then what advantages do
more odorous males have?
The situation is further complicated by the fact that olfactory
acuity and specificity is modulated by the menstrual cycle [67].
Both acuity and sensitivity to putative human male pheromones
appears to peak at ovulation. Schneider [68]
proposed that females have a higher olfactory acuity at ovulation
and Doty, Snyder, Huggins and Lowry [69] showed
a direct correlation between estrogen levels, LH levels, and
heightened olfactory sensitivity. These changes in olfaction
during the menstrual cycle extend well to the odor of androstenol,
and in general to the more "musky" odors typical of
males. Benton [70] showed that the application
of androstenol to the upper lip of females made them rate their
mood at the time of ovulation as more submissive. In contrast,
Filsinger and Monte [71] found no clear link
between sexual history and the perception of androstenone. However,
the absence of a correlate might well be explained by research
design that did not discriminate between females who take hormonal
contraceptives and those who do not, since the estrogen component
of contraceptive hormones can be expected to influence olfactory
ability. Quite notable, however, is that nearly all studies
have found that androstenone is rated negatively independent
of the female cycle.
These mixed findings do not rule out the possibility that the
female hormonal status may directly influence the perception
of androstenone and androstenol. Maiworm [64]
found that at different periods in the menstrual cycle androstenone
and androstenol had different effects. Contrary to expectations,
these substances showed no effect during the middle period of
the menstrual cycle, in which ovulation is possible. Rather,
effects are greatest during the first period of the menstrual
cycle. At the same time, both pleasant and less pleasant effects
may be observed in the final period of the cycle.
Overall, results suggest the existence of two different olfactory
signals: androstenol, which induces female attraction to males,
and androstenone, which induces negative emotions in females.
The functional assessment of such a positive-negative mood-inducing
signal requires consideration of a set of evolutionary hypotheses.
Pheromones
and the battle of the sexes
Parental
investment theory [65] predicts that females
who look for long-term relationships 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 with as many fertile
females as possible, or to develop a pair bond. This helps to
ensure that either a large number of offspring survive without
significant paternal investment, or that paternal 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 would favor
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 ubiquitarian sex specific differences in mate selection criteria
[72] attests that male and female cognition
is adapted to the biological constraints of mate selection.
For example, neither males nor females consciously perceive
human ovulation. Since ovulation is associated with a number
of overt physiological and behavioral changes, it is surprising
that it is not consciously detected. However, olfactory perception
is one "unconscious" mechanism that is associated
both with the physiological and behavioral changes of the menstrual
cycle. Alexander and Noonan [73] and also
Symons [74] have argued that concealed ovulation
evolved because females need to trick males into forming a bond.
Males who were not aware of optimal (i.e., ovulatory) female
fertility would remain bonded to ensure impregnation and paternity.
A female who provided cues to ovulation might risk losing paternal
investment, due to paternal uncertainty and limited temporal
reproductive interaction. This hypothesis implicates male fear
of cuckoldry as an evolutionary pressure [65].
One evolutionary outcome would be that the females ability
to secure paternal care is affected by mechanisms that increase
temporal aspects of the pair bond and enhance male confidence
of paternity. Concealed ovulation is a mechanism that fits this
hypothesis.
In contrast, Benshoff and Thornhill [75] as
well as Symons [74] have proposed an alternative
evolutionary scenario where concealed ovulation evolved to increase
the chances of successful cuckoldry by females so they "can
escape the negative consequences of being pawns in marriage
games" [76]. Once monogamy is established,
a female's best strategy would be to copulate outside the pair
bond because she could then obtain superior genes with a certain
expectation of paternal investment, and the increased survival
of genetically superior offspring. These two hypotheses imply
different impacts of heritable traits. If genes, which induce
paternal care, were relevant for offspring success, a male paternity-securing
function for concealed ovulation would be possible. If there
were other traits not related to paternal care but relevant
to offspring survival, then concealed ovulation would allow
females to exploit occasional opportunities to mate outside
the pair bond [77]. In both cases, overt cues
of ovulation may be selected against because it would hinder
the female's mating strategies [73, 78].
The second hypothesis has received considerable support from
Bellis and Baker [79]. They conducted a study
of 2708 females and found those 13.8% of 145 "unprotected"
extra-pair copulations (EPC) occurred during the ovulatory phase
of the menstrual cycle and were preceded in most cases by intra-pair
copulations (IPC). EPCs were rarely followed by IPCs. According
to his study EPCs, and thus, female infidelity peak 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. It is still unclear what proximate mechanism or mechanisms
cue female EPC at ovulation. The possibility has been raised
[80] that conditioning might facilitate response
to sexual stimulation should it first be encountered during
the follicular phase. In this regard, pheromonal stimuli from
a male, first encountered during ovulatory sexual intercourse,
might help to neuroendocrinologically condition a female's sexual
response. Similarly, pheromonal stimuli from a female, first
encountered during ovulatory sexual intercourse, might help
to neuroendocrinologically condition a male's sexual response,
and help to ensure properly timed reproductive sexual behavior
[81]. In any case, 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 deceptive attempts by females to conceal ovulation.
Grammer [82] described a possible male counter
strategy: the evolution of the androstenone-androstenol signaling
system. In a study, 290 female subjects rated the odor of androstenone.
A change in assessment throughout the menstrual cycle was found:
ovulatory women found the scent of androstenone, the most dominant
odor 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 [64], which were of borderline
significance. Male body odor is usually perceived as unattractive
and unpleasant by females but this evaluation changes when conception
is most likely, and androstenone, minimally, becomes less aversive.
This finding is underlined by the fact that anosmia to androstenone
also varies with cycle. With optimal likelihood of conception,
we find fewer anosmic females [82].
It seems possible that changes in the ability to perceive musky
male odors during the menstrual cycle could also be a female
strategy, although more data need to be gathered to support
this hypothesis. However, the change in female attitude towards
male body odor can be expected to impact mate selection and
perhaps self-initiated copulations by females. With regard to
the androstenol-androstenone signaling system, the situation
for androstenol seems clear - it makes males more attractive
to females. But females are less likely to act on this olfactory-based
attraction unless fitter males produce more androstenol.
The situation is more complicated because producing androstenol
inevitably produces androstenone. The androstenone production
has a disadvantage because of its unpleasantness. 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
odor. Thus the attractiveness-enhancing component of the smell
does not seem to be the main, or at least only, function of
the signaling system. Regarding androstenone, the fact that
ovulatory females assess its odor as more pleasant could be
advantageous for males, as odorous males would 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 concealed ovulation. The concept of ovulation
radar fits our hypotheses about affective reactions. For example,
a pheromone from the male elicits change in the hormonal milieu
of the female. However, the female is not aware of this change,
even though the hormonal change affects her behavior. Similarly,
pheromones from the female elicit changes in the hormonal milieu
of the male that affect his behavior by chemically signaling
him that the female is ovulating. Females faced with an evolved
male strategy to detect concealed 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. Other mammalian males, including
non-human primates (especially rhesus monkeys) perceive both
estrogen-related reproductive fitness and ovulation through
olfaction. 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 [83]. Furthermore, rhesus
males show no interest in ovariectomized rhesus females, presumably
because ovariectomized rhesus females lose the odor characteristic
of higher estrogen levels at ovulation. Rhesus males regain
interest in copulation when the vaginal secretions from intact
(e.g., estrogenized) 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 estrogen-based
chemical signaling system might also exist in humans [84,
85, 86, 87].
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 [88].
The behaviorally active fraction of the rhesus vaginal secretions
- referred to as "copulins" - consists of volatile,
short-chained fatty acids [89]. 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 [85]. In addition, the composition
of these copulins varies during the menstrual cycle. Preti and
Huggins [86] confirmed this observation. Cowley,
Johnson, and Brooksbank [90] 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, Ford, and Preti [91]
used a questionnaire to evaluate the intensity and pleasantness
of different vaginal fluids from a complete menstrual cycle.
They found that odor at ovulation was both the most intense
odor, and the least unpleasant odor.
Juette [43] synthesized female vaginal secretions
("copulins") and tested for their ability to act as
chemical signals for males. Menstrual, ovulatory and pre-menstrual
fatty acid compositions of copulins and an odorless water control
were presented to 60 non-smoking male subjects for 25 minutes
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. Ovulatory fatty acid compositions
stimulated male androgen secretion and changed the discriminatory
cognitive capacities of males with regard to female attractiveness.
Males became less discriminating. Therefore the copulins may
act as putative human pheromones and provide beautifully balanced
"strategic weapons" in the "battle of the sexes"
and the "war of signals" resulting from sex differences
in parental investment theory.
However, it is not necessary to view these "battles"
or "wars" only from the perspective of parental investment
theory. Mammalian pheromones ensure properly timed reproductive
sexual behavior in many species. It should surprise no one that
pheromones would be involved in properly timed human reproductive
sexual behavior. If one examines what is known about the interaction
between pheromones and our neuroendocrine system, there is support
for the extension of mammalian olfactory communication to human
behavior. First and foremost is the effect of mammalian pheromones
on conspecifics of the opposite sex: the LH increase and reported
ovulatory increase in male T, for example. Persky, Lief, OBrien,
Straus, and Miller [92] commented on the observed
ovulatory increase in T levels of human males, and suggested
that, somehow, the female was signaling the male that she had
ovulated, and that he responded, like a male rhesus monkey with
an increase in T. Morris, Udry, KhanDawood, & Dawood [93]
replicated this work and described their findings as an unobserved
event that causes increased intercourse. Though neither of these
studies specifically mentioned human pheromones, affective reactions
were present both in the male and in the female, and pheromones
are the most likely cause of the affective reactions. For example,
the increased T in the male can readily be linked to increased
intercourse, whether or not the increased T was an observable
event. Finally, Singh & Bronstad [81]
showed that human males find the natural body odor of ovulatory
females to be most pleasant, when compared to the natural body
odor during other phases of the menstrual cycle. The male's
hedonic rating of pleasant ovulatory odor; the increased T,
and the increased intercourse, collectively offer significant
support for the concept that chemical communication is more
important to properly timed reproductive sexual behavior than
is visual or other sensory input. If, for example, male canines
were able to tell us that they preferred the scent of estrus
odor, and estrus odor increased male T, we would readily explain
the affective reaction of the "bitch in heat" which
correlates with increased copulation.
Because sexual activity is not limited to the ovulatory phase
of the menstrual cycle, human sexual behavior is considered
to be more complex than that of other mammals who depend upon
properly timed reproductive sexual behavior for species survival.
There are other cues, besides chemical cues, that are involved.
However, it is remarkable that many people consider visual cues
to be more important than olfactory cues, when consideration
is given for the mammalian mechanisms that ensure properly timed
human reproductive sexual behavior.
Pheromones
as honest signals in mate selection
It
is presumable that human scent, apart from the above-mentioned
functions, could - like other cues in mate selection - also
signal aspects of reproductive fitness. Several studies have
found that bodily and facial symmetry play a role in attraction
and thus in choice criteria for human mating. Symmetry is believed
to signal developmental stability, which refers to an individual's
ability to cope with genetic and environmental perturbations
during early development. Recent research has focused on the
significance of developmental stability as mate choice-criterion.
Sex steroid hormone dependent human body odor could transmit
information about an individual's developmental stability as
an additional, redundant olfactory signal. Since olfactory and
visual cues have different physiological roots, the signaling
errors are likely to be uncorrelated. Thus, taking the information
of both signals into account reduces the error and allows much
more reliable mate choice decisions (see [94]
for details).
Rikowski and Grammer [95] compared ratings
of body odor, attractiveness, and measurements of facial and
bodily asymmetry of 16 male and 19 female subjects. Subjects
wore a T-shirt for three consecutive nights under controlled
conditions. One group of opposite-sex raters then judged the
odor of the T-shirts, and another group evaluated portraits
of the subjects for attractiveness. Additionally, bodily and
facial symmetry of the odor-donors were measured. Facial attractiveness
and sexiness of body odor showed a significant positive correlation
for female subjects. In men, the situation was different. Positive
associations between body odor and attractiveness and negative
associations between odor and bodily asymmetry could only be
found if female odor raters were in the most fertile phase (i.e.,
ovulatory phase) of their menstrual cycle. Thus, simply put,
ovulatory women preferred the scent of symmetry.
This effect, replicated by Gangestad & Thornhill [96],
could be explained by the above-mentioned female preference
of androstenone around ovulation. Metabolic pathways suggest
a link between a-androstenes and testosterone [97].
It is presumed that only individuals with high immunocompetence
can afford the immune-suppressing effect of a high testosterone
level [98]. Immunocompetence appears to correlate
with high developmental stability [99]. Thus,
human pheromones could indeed be regarded as honest signals
for human mate choice based on the testosterone-immunocompentence-developmental
stability link to pheromone production.
In humans, female olfactory preferences also seem to induce
disassortative mating for components of the major histocompatibility
complex (MHC) as is observed in other mammals [100].
In other words, olfactory cues may be able to reflect parts
of an individual's genome, and body odor seems to influence
female mate choice in order to find a partner who possesses
fitting MHC-dependent immune system components. Simply put,
ovulatory women seem to prefer the scent of genetic diversity.
Indeed, both women who are not taking oral contraceptives, and
men rate similar genetically determined odors as less attractive
than dissimilar genetically determined odors. Thus, not only
are men and women able to distinguish among genetically distinct,
self versus non-self odors, they prefer the scent of non-self
(i.e., genetic diversity) [101]. Men and
women with shared markers of genetic diversity also select perfumes
that may amplify body odor that is linked to their genetic diversity
[102].
Johnston, Hagel, Franklin, Fink and Grammer [103]
propose that male facial attractiveness is mediated by hormones,
and generally support a hormonal theory of facial attractiveness
dependent on the interaction between visually displayed hormone
markers and the hormonal state of the viewer. There is no biological
pathway that directly links visual input either to neuroendocrine
function, or to the hormonal state of the viewer, and male and
female visual systems are not sexually dimorphic. Accordingly,
the means and biological mechanisms by which sexually dimorphic,
hormone-dependent facial features become attractive have yet
to be detailed. However, the olfactory pathways link the hormonal
state of the "viewer" to chemical signals of reproductive
fitness that correlate well with the degree of hormone-dependent,
sexually dimorphic facial features. For example, higher T levels
correlate with the visual appeal of a "stronger" jaw.
The interaction of these visually displayed hormone markers
of reproductive fitness and the effects of the hormones on pheromone
production and distribution suggest that the effects of pheromones
on reproductive neuroendocrine function might provide a critical,
well-detailed, mammalian link between hormone-mediated facial
signals and what we consciously perceive as facial attraction.
We would be remiss if we failed to address yet another aspect
of what is most commonly believed to be visually perceived physical
attraction: the waist-to-hip ratio (WHR) Sex steroid hormones
control regional fat distribution [104],
which interacts with reproductive control mechanisms. For example,
fat tissue converts androgens to estrogens [105].
Circulating E levels appear to lower WHR, while circulating
T levels appear to increase WHR, which is believed to signal
reproductive fitness in women, and perhaps in men [106].
In addition, high levels of LH and FSH as well as estradiol
levels are linked to lower WHR and to the earlier pubertal endocrine
activity of females. However, the conscious or unconscious mechanisms
linked to the perception of WHR and its link to physical attractiveness,
have not been detailed. Presumably, these mechanisms exist cross-culturally,
but they have defied explanation. The conditioning of visually
perceived physically attractive WHR by association with steroid
hormone-dependent chemical cues (e.g., human pheromones) seems
to be a very likely explanation for the increased desirability
of men and women whose weight and height are proportionate.
Each example above, of symmetry, genetic diversity, hormone-mediated
facial attraction, and of WHR, has some as yet undetermined
link to what we visually and consciously perceive to be attractive.
The simplistic statement, we think about what we see and decide
whether or not it is attractive, summarizes these examples.
In contrast, other mammals don't think but somehow manage both
to decide and to choose for genetic and hormonal traits of reproductive
fitness.
In other mammals, links among olfactory acuity and specificity,
genetically determined odors, and hormones and odor production
provide clear examples of affective primacy, like the chemical
cues that affect GnRH-directed hormone responses in limbic structures.
This impact of these chemical cues on hormones allows for rapid
responses, and accurate choices that do not require cognition.
For example, unconscious odor cues link genetic diversity and
all aspects of hormone-mediated mate choice. Affective primacy
is best explained by mammalian, including human, olfactory acuity
and specificity. The explanatory power of visual input pales
by comparison.
Conclusion
We
have addressed several aspects of what is consciously perceived
to be visual attraction both from an ethological and neuroendocrinological
approach. In other mammals, the olfactory link among hormones,
pheromones, and a conspecific's hormones and behavior would
readily establish that visually perceived facial attractiveness,
bodily symmetry, attractive WHRs, and genetically determined
HLA attractiveness, are due to the neuroendocrinological conditioning
of visual responsivity to olfactory stimuli. Yet, we have merely
scratched the surface with regard to the pheromonal basis of
human mate choice. As we can "see", the model of humans
being primarily visual creatures may require some reconsideration.
Human life and interactions are influenced by pheromones whether
or not affect or effect are part of our consciousness. The affective
hormonal reactions caused by olfaction and pheromones dominate
social interaction, and these affective reactions may be the
primary influence on social interactions.
Human pheromones have more potential than any other social environmental
sensory stimuli to influence physiology and, therefore, behavior.
Predictably, we will soon address other aspects of human attraction,
and social confounds such as the paraphillias - and even sexual
orientation in future discourse. Finally, we might even address
the obvious question of how our everyday social lives and future
human reproductive success will be affected by the modern striving
for cleanliness and the reduction of natural body odor.
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