Body odour and sexual attraction

There is a correlation between mate choice, odour preference and genetic similarity at the MHC.[10] Unique body smells are heavily influenced by MHC; these olfactory cues are probably involved in mate choice and preferences.[11]

The Major Histocompatibility Complex (MHC) shown presenting peptides to the immunological defence cells

MHC is expressed codominantly; a more diverse set of MHC genes leads to a stronger immune system.[12] Women prefer male partners with differing MHC genes from themselves. An evolutionary explanation is that females are attracted to males with MHC alleles different from their own, to provide their offspring with a stronger immune system.[13]

Females not using hormonal contraceptives were more attracted to the scent of males with dissimilar MHCs. Females currently using hormonal contraceptives preferred the scent of men with MHCs similar to their own.[14] The scent of an individual with low fluctuating asymmetry is universally more attractive.[15]

The increased attraction between people of dissimilar MHCs may help to prevent incest and subsequent birth defects.[16] This inbreeding avoidance hypothesis proposes that biases towards heterozygotic alleles prevent harmful genetic consequences which can arise from mating with genetic family members. Olfactory cues can be used to recognise kin.[17]

Couples who have many failed attempts at conception share a considerably larger amount of genes than those who are able to conceive without problems.[18] If, for these genetically similar couples, there is a successful conception, the babies are often born early or underweight.[19]

A third hypothesis explaining the function of dissimilar MHC mate preferences, the parasite hypothesis, suggests that MHC heterozygotes may be resistant to rapidly evolving parasites.[13]

The human leukocyte antigen system is a gene complex which encodes MHC in humans. Over thirty olfactory receptor genes have been located at the HLA class I region,[20] which presents peptides from inside the cell to be destroyed by the immune system. HLA- linked olfactory receptor genes can therefore provide a possible mechanism for detecting HLA- specific odours.[21]

Androstenol, found in fresh male sweat, is attractive to women.

Men and women are attracted to the pheromones they produce and HLA is related to the perceptions of other peoples' odours.[22] Males produce androstenol and androstenone. Androstenol is produced by fresh male sweat and is most attractive to women, while androstenone is produced once the sweat is exposed to oxygen and is highly unpleasant to women.

Studies have shown that women who are at the most fertile stage of their menstrual cycle prefer the smell of men that have higher testosterone levels.[23] Heterozygosity of HLA can also be detected through scent: in this case, heterozygosity confers greater ability to recognize a wider variety of antigens. Females, especially when not using hormonal contraceptives, are more attracted to the scent of males heterozygous for HLA.

Androstenone, from stale male sweat, is unattractive.

However, the same attraction and mate preferences are not held by males for heterozygous females. Males are, however, more attracted to the scent of females with rare HLA alleles.[24] Men's arousal can be influenced by a variety of odours. For example; pumpkin pie, liquorice, doughnuts, and lavender can increase penile blood flow consequently causing arousal.[25]

Two types of male pheromones: 5α-androst-16-en-3-one (MP1, androstenone) and 4,16-androstadien-3-one (MP2, androstadienone) and one type of female pheromone: 1,3,5(10),16-estratetrael-3-ol (FP, estratetraenol) are used as signals of mating quality. Studies[26] showed that MP2 has the strongest response produced by female vomeronasal organ (VNO), which is the first stage of the olfactory system. Sex-difference processing in the hypothalamus has been found between female and male pheromone, including in the VNO, where opposite-sex pheromones have different surface potential.[26][27][28] Studies have illustrated a relationship between human facial attraction and pheromones.[29] Individuals rated those of the opposite sex as more attractive if they preferred the individuals pheromones odour. It was also demonstrated that partners in a long-term relationship would have higher concordance between two types of signals of mating quality, vision and olfaction. In addition, no difference was found between two types of male pheromones in women's preference aside from the location of pheromones production.

In contrast to previous results reported in the literature, it has also been found that odours perceived from a female in follicular phase were actually considered more pleasant and sexier by males than odours perceived from that female in the luteal phase. Researchers discovered that the persistence of the menstrual cycle-dependent olfactory identification was extensive. However, the possibility of odours in the living environment overwhelming the menstrual cycle-dependent odours was not ruled out.[3] Repeated exposure to the specific odours increases the threshold level of odour detection and therefore reduces the stimulation in humans.[34] Additionally, it has been proposed through research that male in a relationship would be more sensitive to their partner's onset of ovulation-linked odour, and resultantly become desensitised after repeated exposure. On the other hand, non-paired males were continuously sensitive to the odour.[3] This demonstrates the persistence of the odour as an evolutionary or adaptation process, which could ensure the offspring reproduction success of female by keeping constant exposure to males during their menstrual cycle. During this period, the most fertile females tend to have more extra-pair copulations.[3][35] Males testosterone levels are found to be associated with a females’ reproduction fertility, such that males exposed to scents of females during the peak period of their fertility, had significantly higher testosterone levels than their baseline levels.[36] Evolution suggests this is an adaptation due to the physical changes inside the male body, although more research must be conducted to ensure these high levels of testosterone lead to reproductive behaviours.

The oral hormone contraceptive pill

Whilst a vast number of studies have been conducted to investigate body odour and mating, research is now shifting in particular towards the effect of male scent to female sexual attraction. This is largely due to the effects of the menstrual cycle and hormone contraceptives, which directly affect women's partner preference. Past research has highlighted the importance of a male's scent to females, such that smell was rated significantly more important for women than men. Furthermore, smell and body odour were rated as the most important physical factor for females, compared to looks for men.[44] Further studies have aimed to understand these sex differences. Using questionnaires and self-report data, a greater reliance was found for females on olfactory cues than males. This reliance was valued for females in both sexual and non-sexual contexts.[45] The research strongly supports the hypothesis that whilst men use more physical and visual cues, women rely more heavily on olfactory cues such as body odour that men tend to overlook.

It has been established that women tend to rely more heavily on olfactory cues than males, rating those with pleasant body odour as more attractive than those with less pleasant body odour. Moreover, body odour and sexual attraction can be enhanced using artificial fragrances and dietary habits. Whilst males are influenced by body odour during selection, past research has demonstrated a significantly greater reliance on such cues by females.

A dependence on such olfactory cues has led to the enhancement of male body odour to influence female attraction. Past research has shown that videos of men using fragranced antiperspirants were rated as more attractive by women than those in a placebo control condition. In addition to this, females gave higher ratings of masculinity than males, particularly in the fragranced condition.[45] This provides evidence that females are more attentive to olfactory cues during partner selection. Aside from artificial fragrances, researchers have also begun to focus on more natural odour enhancements such as diet quality. A recent study aimed to investigate whether a dietary fruit and vegetable intake would influence female mate preferences. Its results showed that subjects rated as most pleasant smelling were those with a higher fruit and vegetable intake, suggesting male body odour can be enhanced by diet to appeal to females.[46]

Both sexes commonly use artificial scents to enhance their perceived sexual appeal. Many of these (musk compounds) share a similar chemical profile with naturally produced body chemicals.[47] Research has found a significant correlation between an individual's MHC genotype and the ratings they assigned to certain perfumes labelled to use "for self".[47] This therefore supports the hypothesis that perfumes can personally enhance body odours that indicate an individual's immunogenetics. However, several infertility issues may arise when people use perfumes or scented body washes that erase their natural scent, hindering women in particular from being able to detect if their partner is genetically comparable.

Insects use extremely sensitive receptors to detect pheromone signals. Each pheromone signal can elicit a distinct response based on the gender and social status of the recipient.[48] In insects, sex pheromones can be detected in very minute concentrations in the environment. Insect sex pheromones, usually released by the female to lure a male, are vital in the process by which insects locate each other for mating.[48] The main purpose of releasing these sex pheromones is to attract a partner from a distance, however the sex pheromones also serve to evoke a courtship response and sexually excite the male prior to copulation.[49] Male insects can also release sex pheromones, but this is only for the purpose of sexually exciting the female, making her more receptive to the male's advances. Generally, the majority of insects are sensitive and selective to the sex pheromone of their own species.

Insects make use of two classes of pheromone signals; the pheromones that induce immediate or releaser effects (for example, aggression or mating behaviours) and those that elicit long-lasting or ‘primer’ effects, such as physiological and hormonal changes.[48]

A pair of mosquitos during mating season

There is a significant amount of research supporting body odour and sexual attraction in insects. Observations and laboratory experiments of Culiseta inornata, identified a chemical substance involved in mating behavior, when exposed to this scent the male mosquitos were found to attempt sex with dead females and when exposed to the scent of virgin females, the males showed increased sexual activity through excited flight, searching and attempts to copulate with other males.[50] Further evidence comes from research on the commercial silkworm moth, Bombyx mori, a chemical produced in the abdominal sac of the female adult moth is released shortly after its emergence from the cocoon, male moths were found to be immediately attracted to this scent demonstrated by a characteristic wing flutter and attempts to copulate.[51] The sex pheromones of the silkworm moths can elicit responses in the male antenna at concentrations of only a few hundred molecules per square centimeter.[52]

For vertebrates, aquatic environments are an ideal medium for dispersing chemical signals over large areas. Aquatic vertebrates use chemical signals for a wide range of purposes, from attracting mates to distant nesting sites during spawning, to signalling reproductive readiness and regulating predator/prey interactions.[48] Research on goldfish has identified that the fish release hormones in various combinations, depending on the reproductive status of the releaser, and these different combinations can elicit varying degrees of male courtship in the recipient.[53]

In terrestrial environments, chemosignals can be either volatile or non-volatile.[48] Accordingly, terrestrial vertebrates have two functionally and anatomically distinct olfactory systems: the main olfactory system, which is receptive to volatile cues, and the vomeronasal system, which is thought to process mostly non-volatile pheromones.[54]

When it comes to sex, mammals use chemical signals (pheromones) to convey information to one another. Mammal's pheromones are air-borne chemical substances released in the urine or feces of animals or secreted from sweat glands that are perceived by the olfactory system and that elicit both behavioral and endocrine responses in conspecifics.[55] Mammals use sex pheromones to arouse, attract, and elicit specific behavioral responses from the opposite sex.[56] In mammals, chemical signals and the scent glands that secrete them have many features in common, for example, expression in only one sex, development only in adults, often only secreted in breeding season and used exclusively in mating.[57] For an odour to be exclusively result in sexual behavior, it must not only be perceived and preferred, but when absent there should be a decrease or complete elimination of sexual activity. This exclusivity has only been shown in golden hamsters[58] and the rhesus monkey.[59]

Mammalian pheromones can elicit both long-lasting effects that alter the hormone levels of the recipient animal, and short-term effects on its behavior.[60] For example, detection of male pheromones by female mice has been found to encourage onset of puberty, however the detection of female pheromones have been found to delay the onset of puberty.[61]

Odour can influence mammalian mating both directly and indirectly. Odour may act as a direct benefit to females, for example by avoiding contagious diseases by using odour cues to choose a healthy mate.[57] Odour can also act as an indicator mechanism, a form of indirect benefit, for example when a male displays a particular trait such as strength of odour which is in proportion to their heritable viability, females choosing males with strong odours will gain genes for high viability to pass to their offspring.[62]

There is vast evidence for the use of pheromones in mating behaviors. For example, when boars become sexually aroused, they salivate profusely dispersing pheromones into the air. These pheromones attract receptive sows, causing it to adopt a specific mating posture, known as standing, which allows the male boar to mount it and therefore copulate.[63]

Regardless of the species, sex pheromones are often structurally similar and for that reason different species need to be able to respond to the correct pheromone. It is the variation in the ratios of each compound within a pheromone that yields species specificity.[64] The use of mixtures of compounds as pheromones is well documented in insects, research into male orchid bees demonstrates that specific odours mediate exclusive attraction within a species.[65]