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Evidence for odour-mediated assortative mating in humans: The impact of hormonal contraception and artificial fragrances

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Abstract

There is substantial evidence for assortative partner preferences in humans based on physical characteristics. In contrast, evidence suggests that olfactory preferences tend to be disassortative, with people preferring body odour of potential partners who are dissimilar at key genetic loci, perhaps to gain fitness advantage through offspring heterozygosity. We compared ratings of perceived body odour similarity of real couples with those of randomly paired 'fake' couples. Contrary to prediction, we find that odours of real partners are perceived more, rather than less, similar to each other than fake couples. However, this applied only to natural odour samples: there were no differences in similarity levels of real and fake couples' samples which were collected while wearing artificial fragrances. Furthermore, in light of suggestions that hormonal contraception (HC) disrupts disassortative odour preferences in women, we compared odour similarity among real couples in which the female partner was using or not using HC at the time when the relationship began. We find that odours of HC-using couples are of intermediate similarity between non-using and fake couples, suggesting that HC use during partner choice could affect odour-influenced assortment. We also examined the association between relationship satisfaction and perceived similarity of unfragranced odours of real couples. We found that these are positively correlated in male partners but negatively correlated in the female partners, indicative of a sex difference in the relative favourability of odour similarity in partner preference. Finally, by comparing odour similarity ratings with those given by perfumers using a novel olfactory lexicon we found evidence that similarity judgements were based on the Spicy/Animalic aspects of individual odour profiles. Taken together, our results challenge the conventional view that odour-mediated partner preferences in humans are typically disassortative.

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Previous studies in animals and humans show that genes in the major histocompatibility complex (MHC) influence individual odours and that females often prefer odour of MHC-dissimilar males, perhaps to increase offspring heterozygosity or reduce inbreeding. Women using oral hormonal contraceptives have been reported to have the opposite preference, raising the possibility that oral contraceptives alter female preference towards MHC similarity, with possible fertility costs. Here we test directly whether contraceptive pill use alters odour preferences using a longitudinal design in which women were tested before and after initiating pill use; a control group of non-users were tested with a comparable interval between test sessions. In contrast to some previous studies, there was no significant difference in ratings between odours of MHC-dissimilar and MHC-similar men among women during the follicular cycle phase. However, single women preferred odours of MHC-similar men, while women in relationships preferred odours of MHC-dissimilar men, a result consistent with studies in other species, suggesting that paired females may seek to improve offspring quality through extra-pair partnerships. Across tests, we found a significant preference shift towards MHC similarity associated with pill use, which was not evident in the control group. If odour plays a role in human mate choice, our results suggest that contraceptive pill use could disrupt disassortative mate preferences.
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The major histocompatibility complex (MHC, called HLA in humans) is an important genetic component of the immune system. Fish, birds and mammals prefer mates with different genetic MHC code compared to their own, which they determine using olfactory cues. This preference increases the chances of high MHC variety in the offspring, leading to enhanced resilience against a variety of pathogens. Humans are also able to discriminate HLA related olfactory stimuli, however, it is debated whether this mechanism is of behavioural relevance. We show on a large sample (N = 508), with high-resolution typing of HLA class I/II, that HLA dissimilarity correlates with partnership, sexuality and enhances the desire to procreate. We conclude that HLA mediates mate behaviour in humans.
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Cultural practices may either enhance or interfere with evolved preferences as predicted by culture-gene coevolution theory. Here, we investigated the impact of artificial fragrances on the assessment of biologically relevant information in human body odor. To do this, we examined cross-sensory consistency (across faces and odors) in the perception of masculinity and femininity in men and women, and how consistency is influenced by the use of artificial fragrance. Independent sets of same and opposite-sex participants rated odor samples (with and without a fragrance, N = 239 raters), and photographs (N = 130) of 20 men and 20 women. In female, but not male raters, judgments of masculinity/femininity of non-fragranced odor and faces were correlated. However, the correlation between female ratings of male facial and odor masculinity was not evident when assessing a fragranced body odor. Further analysis also indicated that differences in ratings of male odor masculinity between men with high and low levels of facial masculinity were not present in fragranced body odor samples. This effect was absent in ratings of female odors by both female and male raters, suggesting sex-specificity in the effects of fragrance on odor perception. Our findings suggest that women may be more attentive to these odor cues, and therefore also to disruption of this information through fragrance use. Our results show that cultural practices might both enhance and interfere with evolved preferences.
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Research has shown that human partners are more similar than expected by chance on a variety of traits. Studies examining hair and eye colour show some evidence of positive assortment. Positive assortment may reflect attraction to self-similar characteristics but is also consistent with attraction to parental traits. Here, we examine self-reported partner hair and eye colour and the influence that own and parental colour characteristics have on these variables. Parental characteristics were found to correlate positively with actual partner characteristics for both men and women. Regression analysis predicting partner characteristics from maternal and paternal traits (which controls for own traits) revealed the greater importance of the opposite-sex parent over the same-sex parent in predicting both hair and eye colour of actual partners. The findings may reflect an influence of parental colour characteristics on human partner choice. Attraction to opposite-sex parental characteristics is seen in a wide variety of animals where it is usually attributed to imprinting processes in infancy. Although the mechanism is unclear and not necessarily confined to infancy, the data reported here are consistent with a somewhat analogous process to imprinting occurring in humans.
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Matings between close relatives often reduce the fitness of offspring, probably because homozygosity leads to the expression of recessive deleterious alleles1, 2, 3, 4, 5. Studies of several animals have shown that reproductive success is lower when genetic similarity between parents is high4, 5, 6, 7, and that survival and other measures of fitness increase with individual levels of genetic diversity8, 9, 10, 11. These studies indicate that natural selection may favour the avoidance of matings with genetically similar individuals. But constraints on social mate choice, such as a lack of alternatives, can lead to pairing with genetically similar mates. In such cases, it has been suggested that females may seek extra-pair copulations with less related males4, but the evidence is weak or lacking4, 5. Here we report a strong positive relationship between the genetic similarity of social pair members and the occurrence of extra-pair paternity and maternity ('quasi-parasitism') in three species of shorebirds. We propose that extra-pair parentage may represent adaptive behavioural strategies to avoid the negative effects of pairing with a genetically similar mate.
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People are able to assess some personality traits of others based on videotaped behaviour, short interaction or a photograph. In our study, we investigated the relationship between body odour and the Big Five personality dimensions and dominance. Sixty odour samples were assessed by 20 raters each. The main finding of the presented study is that for a few personality traits, the correlation between self-assessed personality of odour donors and judgments based on their body odour was above chance level. The correlations were strongest for extraversion (.36), neuroticism (.34) and dominance (.29). Further analyses showed that self–other agreement in assessments of neuroticism slightly differed between sexes and that the ratings of dominance were particularly accurate for assessments of the opposite sex. Copyright © 2011 John Wiley & Sons, Ltd.
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The variety of interpersonal relationships in contemporary society necessitates the development of brief, reliable measures of satisfaction that are applicable to many types of close relationships. This article describes the development of such a measure. In Study I, the 7-item Relationship Assessment Scale (RAS) was administered to 125 subjects who reported themselves to be "in love." Analyses revealed a unifactorial scale structure, substantial factor loadings, and moderate intercorrelations among the items. The scale correlated significantly with measures of love, sexual attitudes, self-disclosure, commitment, and investment in a relationship. In Study II, the scale was administered to 57 couples in ongoing relationships. Analyses supported a single factor, alpha reliability of .86, and correlations with relevant relationship measures. The scale correlated .80 with a longer criterion measure, the Dyadic Adjustment Scale (Spanier, 1976), and both scales were effective (with a subsample) in discriminating couples who stayed together from couples who broke up. The RAS is a brief, psychometrically sound, generic measure of relationship satisfaction.
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Individuals in some species prefer mates carrying dissimilar genes at the major histocompatibility complex (MHC), which may function to increase the MHC or overall heterozygosity of progeny. Here I review the evidence for MHC-dependent mating preferences from recent studies, including studies on the underlying olfactory mechanisms and evolutionary functions. Many studies indicate that MHC genes influence odour, and some work is beginning to examine the potential role of MHC-linked olfactory receptor genes in mating preferences. MHC-dependent mating preference increases the MHC-heterozygosity of progeny, which is suspected to confer resistance to infectious diseases. In humans, heterozygosity at MHC loci is associated with increased resistance to hepatitis and HIV infections, but experimental evidence for the heterozygote advantage hypothesis has been lacking. Here I re-analyse data from previously published experimental infection studies with mice. I show that although overdominance is rare, resistance is often dominant, suggesting that heterozygotes are often protected. A second (nonmutually exclusive) possibility is that MHC-disassortative mating preferences promotes inbreeding avoidance. This hypothesis is supported by recent evidence that MHC genes play a role in kin recognition, and that mating with close kin has rather deleterious fitness consequences. In conclusion, I discuss other ways that MHC genes might influence sexual selection. The research on MHC-mediated mating preferences is integrating the study of animal behaviour with other seemingly disparate fields, including sensory biology and immunogenetics.
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Females of a number of primate species display their fertile period by behavioural and/or morphological changes. Traditionally, the fertile period in human females has been considered to be concealed. However, this presumption has rarely been tested. One of the possible mechanisms for assessing menstrual cycle phase is through the sense of smell. In this study possible changes in odour across the menstrual cycle were investigated. Samples of body odour were acquired from 12 women (aged 19–27 yr), none of whom were using hormonal contraceptives. Samples were collected using cotton pads worn in the armpit for 24 h, from the menstrual, follicular and luteal cycle phases. Our experimental sample of 42 males (age 19–34 yr) repeatedly rated these odour samples for their intensity, pleasantness, attractiveness and femininity. Raw subjective smell ratings from each man were transformed to z-scores. Subsequently, these z-scores were tested by the general linear mixed-model analysis (PROC MIXED, SAS) with the female's ID nested within the subject's ID as a random factor to account for the repeated measures of the subjects. Significant changes across the cycle were found for ratings of pleasantness [F(2,689) = 702; p = 0.001], attractiveness [F(2,546) = 6.35; p = 0.002] and intensity [F(2,530) = 3.57; p = 0.028]. Odour from women in the follicular (i.e. fertile) phase was rated as the least intense and the most attractive. Subsequent post hoc analysis revealed significant differences in intensity, pleasantness and attractiveness between the menstrual phase and the follicular phase, and in pleasantness and attractiveness between the menstrual and luteal phases. Significant difference between the follicular and the luteal phase was found only for attractiveness. Our results suggest that men can potentially use smell as a mechanism for monitoring menstrual cycle phase in current or prospective sexual partners. Therefore, the fertile period in humans should be considered non-advertized, rather than concealed.
Article
Similar criteria may operate in mate choice and in mate retention. For example, United States couples tend to be similar, and the more similar they are, the happier and more stable their relationships are. Another widespread criterion is male dominance, which females in several primate species seem to find desirable in a mate. Defined in various ways, dominance seems to characterize men that women find desirable. Also, cross-cultural evidence suggests that attractiveness, particularly in women, enhances mate value. A survey of over 1000 British couples was undertaken to test the homogamy (similarity), male dominance, and female attractiveness hypotheses in that society. In 19 of 42 tests, homogamous couples tended to be significantly (p < 0.01) more satisfied. Couples, especially wives, were more satisfied if the husband dominated decision making, but excessive husband dominance reduced satisfaction. Husbands were more satisfied if the wife was moderately more attractive than they were. Unlike some previous U.S. studies, this one revealed no relationship between marital satisfaction and the husband's earning more than the wife, being better educated, or having wealthier parents. In addition to the homogamy hypothesis, the notion that dominant men gain attractive wives received qualified support. Economic factors may be less fundamental to marital satisfaction than these other variables.
Article
Previous theoretical and empirical studies have shown that individuals may act to the benefit of others of similar genotype. We argue that the ability to discriminate among individuals of varying degrees of relatedness is prevalent in many species, and that the tendency to favor relatives can be considered a special case of a tendency to favor those of similar genotype. The phenomenon of assortative mating can be explained in this way, but new evidence capable of disproving this conjecture is not easily obtained. We have reanalyzed three previously reported studies of heritability and assortive mating in humans, and show that there is a greater degree of assortative mating on more highly heritable traits, in accordance with the prediction.
Article
Dating and married couples show comparable levels of assortment for physical traits. Married couples, however, are more assorted on psychological traits. It is argued that both dating and married couples initially assort on physical similarity, but that couples who are similar on psychological traits are more likely to marry. Physical traits are apparently critical in initial partner selection; psychological traits are more important for long-term relationships. There is little evidence that couples become more similar in psychological traits over time, implying that existing similarities are due to initial assortment.
Article
Whereas the hypothesis of genetically mediated homogamy has been supported by several studies, certain theoretical and methodological criticisms have been raised against genetic similarity theory. As an alternative approach to assortative mating, we suppose that imprinting-like mechanisms, rather than “direct” genetic detection, are responsible for choosing similar spouses. In a study aimed at comparing more than 300 facial photographs of family members and controls, the judges correctly matched wives to their mother-in-law at a significantly higher rate than expected by chance. Furthermore, a higher degree of similarity was ascribed between the husbands’ mother and the husbands’ wife than between the husbands and their wives. A regression analysis has revealed that men who had been more frequently rejected by their mother during childhood were less likely to choose mates who resemble their mothers in physical appearance. These results suggest that under the influence of childhood experiences, sons internalize their mother’s phenotype as a template for acquiring similar mates.
Article
It has become difficult to find a matching perfume. An overwhelming number of 300 new perfumes launch each year, and marketing campaigns target pre-defined groups based on gender, age or income rather than on individual preferences. Recent evidence for a genetic basis of perfume preferences, however, could be the starting point for a novel population genetic approach to better match perfumes with people's preferences. With a total of 116 participants genotyped for alleles of three loci of the major histocompatibility complex (MHC), the aim of this study was to test whether common MHC alleles could be used as genetic markers to segment a given population into preference types. Significant deviations from random expectations for a set of 10 common perfume ingredients indicate how such segmentation could be achieved. In addition, preference patterns of participants confronted with images that contained a sexual communication context significantly differed in their ratings for some of the scents compared with participants confronted with images of perfume bottles. This strongly supports the assumption that genetically correlated perfume preferences evolved in the context of sexual communication. The results are discussed in the light of perfume customization.
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Three very large, nationally representative samples of married couples were used to examine the relative importance of 3 types of personality effects on relationship and life satisfaction: actor effects, partner effects, and similarity effects. Using data sets from Australia (N = 5,278), the United Kingdom (N = 6,554), and Germany (N = 11,418) provided an opportunity to test whether effects replicated across samples. Actor effects accounted for approximately 6% of the variance in relationship satisfaction and between 10% and 15% of the variance in life satisfaction. Partner effects (which were largest for Agreeableness, Conscientiousness, and Emotional Stability) accounted for between 1% and 3% of the variance in relationship satisfaction and between 1% and 2% of the variance in life satisfaction. Couple similarity consistently explained less than .5% of the variance in life and relationship satisfaction after controlling for actor and partner effects.
Article
Extremely high variability in genes of the major histocompatibility complex (MHC) in vertebrates is assumed to be a consequence of frequency-dependent parasite-driven selection and mate preferences based on promotion of offspring heterozygosity at MHC, or potentially, genome-wide inbreeding avoidance. Where effects have been found, mate choice studies on rodents and other species usually find preference for MHC-dissimilarity in potential partners. Here we critically review studies on MHC-associated mate choice in humans. These are based on three broadly different aspects: (1) odor preferences, (2) facial preferences and (3) actual mate choice surveys. As in animal studies, most odor-based studies demonstrate disassortative preferences, although there is variation in the strength and nature of the effects. In contrast, facial attractiveness research indicates a preference for MHC-similar individuals. Results concerning MHC in actual couples show a bias towards similarity in one study, dissimilarity in two studies and random distribution in several other studies. These vary greatly in sample size and heterogeneity of the sample population, both of which may significantly bias the results. This pattern of mixed results across studies may reflect context-dependent and/or life history sensitive preference expression, in addition to higher level effects arising out of population differences in genetic heterogeneity or cultural and ethnic restrictions on random mating patterns. Factors of special relevance in terms of individual preferences are reproductive status and long- vs. short-term mating context. We discuss the idea that olfactory and visual channels may work in a complementary way (i.e. odor preference for MHC-dissimilarity and visual preference for MHC-similarity) to achieve an optimal level of genetic variability, methodological issues and interesting avenues for further research.