Original ArticleDiet quality and the attractiveness of male body odor
Introduction
Human body odor may provide information to aid mate choice and two functions in this regard have been suggested (Stevenson, 2010). The first concerns inbreeding avoidance (e.g., Weisfeld, Czilli, Phillips, Gall, & Lichtman, 2003) and the second the health status of a potential mate (e.g., Gangestad & Thornhill, 1998). While inbreeding avoidance involves conveying information about genetic identity that must remain stable over time, health-related information is likely to be far more labile. Health may decline during bouts of illness or after injury and – of particular interest here – vary with diet. There is a large and well-developed literature in both humans and animals indicating that certain dietary patterns are associated with better short and longer-term health (e.g., Fardet and Boirie, 2014, Flegal et al., 2005, Mokdad et al., 2004). In humans, one dietary pattern that has been consistently found to be associated with good health is one rich in fruit and vegetables (Willett, 1994, Willett et al., 1995). The principal aim of the study reported here was to determine whether indirect (i.e., from the spectrophotometer) and subjective measures of fruit and vegetable consumption (alongside other dietary components), are associated with a more attractive body odor.
In humans a number of bodily locations generate distinct odors (e.g., hair, mouth, genitals etc). Most attention has been paid to that arising in the axillae. The axillae have the highest density of and largest sized apocrine sweat glands of any location on the body (Schall & Porter, 1991). These glands produce an odorless cocktail of lipids and amino acids that are metabolized by bacteria generating numerous detectable volatiles (Schall & Porter, 1991). The pattern of generated volatiles appears to reflect a person's complement of immune system genes, notably human leukocyte antigens (HLA; Zavazava, Westphal, & Muller-Ruchholtz, 1990). It has been suggested that this HLA-related information may be used to support inbreeding avoidance, by enabling a person to choose a mate with a different HLA-type to self (e.g., for: Ober et al., 1997, Ober, 1999; and against: Hendick and Black, 1997, Ihara et al., 2000). Indeed, people seem to prefer sweat odors from an HLA type dissimilar to self (e.g., Wedekind & Furi, 1997).
The second type of information that human sweat (i.e., axillae secretions) can convey relates to the health status of the emitter. Several animal species are known to use olfactory cues to avoid potential mates who are infected by pathogens (e.g., Kavliers, Colwell, Braun, & Cholersis, 2003). In humans, it is now well established that the odor of sweat can be altered by several disease states (Buljubasic & Buchbauer, 2015). Moreover, people dislike the smell of sweat from individuals who have had their immune system stimulated by injection of lipopolysaccharide (Olsson et al., 2014), suggesting that they can detect and respond appropriately to olfactory cues to pathogen infection.
Diet appears to be another health-related factor that influences body odor and how people respond to it. Differences in diet are clearly detectable in human sweat odors (Fialová, Roberts, & Havlíček, 2013). This has been most clearly illustrated in a study by Havlicek and Lenochova (2006). They experimentally varied the quantity of red meat consumed in male participants' diet by having the participants eat a red meat-rich diet for two weeks, which was either preceded or followed by a largely non-meat diet for two weeks. Female participants judged the men's body odor to smell significantly more pleasant on the non-meat diet, which was characterized by increased intakes of eggs, cheese, soy, fruit and vegetables.
Clearly, an important issue when considering health and diet is to identify what dietary pattern is likely to be indicative of good health. This is an interesting problem because at least for some key food types, what may be beneficial in the current environment may not be the same as what was beneficial in the ancestral environment. This is particularly pertinent to the food types varied in the Havlicek and Lenochova (2006) study (i.e., red meat, other protein sources, and fruit and vegetables). The healthiness of red meat consumption is particularly complicated. The proportion of saturated fat farmed red meat delivers – one cause for recommendations to reduce red meat intake (e.g., Dietary Guidelines for Americans, 2015–2020) – is higher than from wild-caught red meats likely typical of ancestral diets (e.g., Hoffman & Wiklund, 2006). In addition, many alternative protein sources are readily available now, which were not in the ancestral past (e.g., eggs, soy, dairy, legumes). Thus red meat eating in ancestral times may have been far more important to health and survival than in the current environment, and meat eating in the current environment may not reflect the health benefits of meat eating in the ancestral past.
While the health implications of meat consumption are complicated to discern, consumption of fruit and vegetables would seem to be far more consistently associated with good health both in contemporary (e.g., Willett, 1994, Willett et al., 1995) and ancestral environments. It is for this reason that we focus on fruit and vegetable consumption throughout the manuscript. There are likely to be several reasons for the beneficial effects of eating fruit and vegetables, but one that has been consistently identified as important concerns dietary carotenoids. Humans, alongside most animals, are unable to synthesize carotenoids. These are required for two principal purposes: (1) the generation of vitamin A and (2) for protection against reactive oxygen species (ROS) generated by metabolic activity in the body (particularly in the reproductive and immune systems) and exposure to UV light. ROS can damage key biological chemicals such as DNA and proteins (Dowling and Simmons, 2009, Markesbury, 1997). Notably, lower plasma carotenoid levels are associated with greater all cause mortality (Shardell et al., 2011) and with the presence of infection (e.g., Koutsos, Calvert, & Klasing, 2003). Many animal species, notably birds and fish, use greater carotenoid levels as a signal for good health (see Whitehead, Ozakinci, & Perrett, 2012). This may also extend to humans. Several studies have now shown that facial skin color is affected by dietary carotenoids, imbuing it with a yellow hue, which people find attractive (e.g., Lefevre et al., 2013, Stephen et al., 2011). Indeed dietary supplementation with fruit and vegetables results in yellower (Tan, Graf, Mitra, & Stephen, 2015) and more attractive skin (e.g., Whitehead et al., 2012).
The primary aim of this study was to determine whether human body odor – axillary sweat – is judged to have more positive attributes when a person's diet is richer in fruit and vegetables — and therefore richer in carotenoids. To test this hypothesis we obtained sweat samples from male donors whose diet varied in fruit and vegetable intake (amongst other things). These sweat samples were then smelled by female judges who rated their hedonic, intensity and qualitative attributes (i.e., redolence to other odors). Male donors and female judges were used for four reasons: (1) female investment in reproduction is high so they should be especially sensitive to health-related cues in potential mates; (2) women report smell to be more important in attractiveness judgments than men (e.g., Herz & Cahill, 1997); (3) men have larger apocrine glands than women, and their sweat is smellier (Doty, Orndorff, Leyden, & Kligman, 1978); and (4) females outperform men on most olfactory tasks (Brand & Millot, 2001).
Dietary information about the male donors was obtained in two ways. The first method was indirect and involved measuring skin yellowness (CIELab b*) using spectrophotometry, which is highly correlated with plasma carotenoid levels and dietary carotenoid intake (Stahl et al., 1998). Thus measures of skin yellowness can function as a proxy marker for fruit and vegetable consumption (Stephen et al., 2011, Whitehead et al., 2012). Second, participants completed a food frequency questionnaire to establish intakes not only of fruit and vegetables, but of other dietary components as well. This allowed us to address two further questions: First, whether greater meat intake, independent of fruit and vegetable intake, affects sweat attractiveness (Havlicek & Lenochova, 2006). Second, whether any other dietary components are associated with the pleasantness of sweat odor.
Section snippets
Overview
This study consisted of two stages. In stage one, male donors generated a body odor sample and then provided information about their diet. In stage two female judges evaluated these male body odor samples. Approval for the study was received from Macquarie University Human Research Ethics Committee and informed consent was obtained from all participants.
Participants
Potential donors were recruited in several ways so as to try and maximize variability in dietary intakes of fruit, vegetables and meat across
Results
Descriptive statistics for the male donors food frequency data are presented in Table 1. Values here show the mean frequency with each item within a particular food category was consumed and reveal a good deal of variation in intake frequencies across the male donors. The lower part of Table 1 presents the female judges hedonic and intensity evaluations of the male donors body odor. On the liking measure the average score was in the mild dislike region, but response ranged from strong dislike
Discussion
This manuscript tested whether fruit and vegetable intake, measured both indirectly via spectrophotometry and by self-report, was associated with more pleasant smelling male axillary sweat. The female judges were able to reliably evaluate the affective and intensity dimensions of male body odor. We found that their affective evaluations were more positive when smelling sweat from men who had consumed more fruit and vegetables, indexed indirectly by skin spectrophotometry, and this effect was
Supplementary materials
The following are the supplementary data to this article.
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