Original ArticleCarotenoid and melanin pigment coloration affect perceived human health☆,☆☆
Introduction
How health is manifest in physical appearance is important throughout the animal kingdom because appearance influences mate choice. In humans too, health is intimately linked with attractiveness (Jones et al., 2004, Rhodes et al., 2001), yet the cues utilized in such health judgments and their validity are unclear. Most studies of how human facial characteristics are potentially linked to health focus on facial shape (Rhodes et al., 2001, Rhodes et al., 2003), although recent studies have begun to focus on skin color and texture (Fink et al., 2001, Fink et al., 2006, Matts et al., 2007, Stephen et al., 2009, Stephen et al., 2009). In three studies, we investigate the role of skin carotenoid and melanin coloration in providing a cue to a healthy diet. In Study 1, we explore cross-cultural consistency in preferences for skin lightness (L*) and yellowness (b*) by comparing the preferences of a UK-based Caucasian population and a black South African population. In Study 2, we examine the effect of carotenoids, obtained from dietary fruit and vegetable intake and from dietary supplementation, on human skin color. In Study 3, we examine the effect of skin carotenoid and melanin coloration on the perceived health of human faces.
The human face exerts a powerful influence on the impression of others and thus is a good starting point for studying how we judge the health of others. Yet for a health cue to be valid the trait must relate both to perceived health and to an aspect of actual health. Coetzee et al. (2009) found links from facial adiposity both to measures of actual health (respiratory illnesses and blood pressure) and to the perceived health of faces, establishing facial adiposity as a cue to health. Other robustly established facial cues to health in the literature are rare. While facial averageness (Rhodes et al., 2001, Rhodes et al., 2007), symmetry (Fink et al., 2006, Grammer & Thornhill, 1994, Jones et al., 2001, Penton-Voak et al., 2001, Rhodes et al., 2001, Rhodes et al., 2007) and female facial femininity (Law Smith et al., 2006, Rhodes et al., 2003, Rhodes et al., 2007) are perceived as healthy, attempts to link these traits to measures of actual health have produced mixed results. Thornhill and Gangestad (2006) found a relationship between female facial femininity and self-reported number and duration of respiratory infections, but Rhodes et al. (2003) found no relationship between female facial femininity and past health from medical records. Similarly, symmetry has been linked with self-reported health measures (Shackelford & Larsen, 1999, Thornhill & Gangestad, 2006), but not with past health assessed from medical records (Rhodes et al., 2001). Averageness predicts childhood health in men and adolescent and current health in women (Rhodes et al., 2001), although this relationship is driven by faces below median averageness (Zebrowitz & Rhodes, 2004).
Recent studies have investigated the contributions of aspects of skin quality, including skin color (Stephen, Law Smith, et al., 2009) and texture (Jones et al., 2004) to the healthy appearance of faces. Both overall skin color (Stephen, Law Smith, et al., 2009) and color distribution (Fink et al., 2006, Matts et al., 2007) are important to perceptions of human health. The role of skin color distribution is outside the scope of this article, however, and we focus on the effects of overall skin pigment coloration on the perceived health of human faces. Previous work has found that skin blood perfusion and oxygenation, which are relatively fast changing causes of skin color, affect the healthy appearance of human faces (Stephen, Coetzee, et al., 2009). In the current article, we concentrate on more stable causes of skin color: melanin and carotenoids.
The CIELab color space is defined by L* (light-dark), a* (red-green) and b* (yellow-blue) color dimensions. It is modeled on the human visual system and designed to be perceptually uniform, a change of one unit appearing to be of approximately the same magnitude regardless of its dimension (Martinkauppi, 2002). Caucasian participants choose to increase the CIELab a* (redness), b* (yellowness) and L* (lightness) values of the skin portions of Caucasian face photographs to enhance apparent health (Stephen, Law Smith, et al., 2009). Here, we evaluate cross-cultural consistency in the perception of increased skin L* and b* values as healthy by comparing the manipulation of Caucasian faces by UK Caucasian participants with the manipulation of black South African faces by black South African participants.
Coloration associated with increased skin blood perfusion and oxygenation can change over a relatively short time scale. Such change primarily increases a* values of the skin and enhances the healthy appearance of faces (Stephen, Coetzee, et al., 2009). Here, we examine the contributions of the other major skin pigments, melanin and carotenoids, to the appearance of faces. Both of these pigment types enhance skin b* values (Alaluf et al., 2002, Stamatas et al., 2004) and induce more long-lasting change in skin color.
Carotenoids cannot be synthesized de novo in the body and are primarily obtained from dietary fruit and vegetables (Alaluf et al., 2002). Carotenoids contribute to human skin b* values through deposition in the skin (Alaluf et al., 2002). Carotenoid concentrations in the skin reflect concentrations in the blood serum and are increased by dietary supplementation, an effect that can be achieved over relatively short courses (within 8 weeks) of dietary supplementation (Stahl et al., 1998), but a direct connection between carotenoid intake and skin color has not been previously reported. We predict that individuals with higher daily carotenoid intakes, from the natural diet or from dietary supplementation, will have increased skin carotenoid deposition and increased skin b* values. We investigate this hypothesis in a dietary study.
Carotenoids are associated with immunocompetence and disease resistance in humans. Supplementation beneficially affects thymus gland growth in children (Seifter, Rettura, & Levenson, 1981) and increases T-lymphocyte number and activity in healthy adults (Alexander, Newmark, & Miller, 1985). Carotenoid levels become reduced in individuals with HIV and malaria, and in individuals with elevated levels of serum α1-antichymotrypsin (an indicator of infection; Friis et al., 2001). The mechanisms of these immune-enhancing properties are unclear, but the antioxidant properties of carotenoids may be involved in neutralizing the high levels of damaging reactive oxygen species (ROS) generated by immune function (Dowling & Simmons, 2009). The benefits from the antioxidant properties of carotenoids may be obtained through the synergistic action of other endogenous or dietary obtained antioxidants such as vitamin C and E (Vinkler & Albrecht, 2010).
Carotenoid deposition in skin may contribute to photoprotection, reducing the level of skin damage caused by both natural and artificial UV light exposure, and increasing the minimum amount of UV exposure required to cause sunburn (minimum erythmal dose; Alaluf et al., 2002, Bouilly-Gauthier et al., 2010).
Carotenoids may also be important in the human reproductive system (Agarwal, 2005, Dowling & Simmons, 2009) as they are in other mammal (Coffey & Britt, 1993) and bird species (Peters, Denk, Delhey, & Kempenaers, 2004). High levels of antioxidants including carotenoids are present in semen and are thought to protect the sperm against ROS produced during meiosis, metabolism and immune processes (Dowling & Simmons, 2009). Seminal carotenoid levels are lower in infertile than in fertile men and carotenoid supplementation improves male fertility (Gupta & Kumar, 2002). Carotenoids may also help to protect the female reproductive system against ROS (Agarwal, 2005).
Theoretically, the use of carotenoids in ornamentation means they are unavailable for immune and detoxification responses (Dowling & Simmons, 2009). Infection with parasites reduces carotenoid levels in guppies and chickens (Olson & Owens, 1998), and nematode infection reduces the brightness of the supra-orbital comb (a carotenoid-based ornament) in red grouse (Martinez-Padilla, Mougeot, Perez-Rodrigues, & Bortolotti, 2007), suggesting that the use of carotenoids in immune defense makes them unavailable for ornamentation. Thus, carotenoid-based ornament color may be a handicapping signal demonstrating superior immunocompetence, explaining their attractiveness to the opposite sex in several bird and fish species (Lozano, 1994). Individuals with superior skills in foraging for carotenoid-rich foods or who need to use less carotenoids in immune or detoxification responses can invest more in ornamentation while still having sufficient for immune defense.
From these considerations of humans and other species, we predict that increased skin carotenoid coloration will enhance the healthy appearance of human faces.
Increased melanin levels increase human skin b* and decrease L* values (Stamatas et al., 2004). Melanin presents health costs and benefits depending on sunlight levels. It is important in photoprotection against skin cancer and sunburn and prevents the photolysis of folate, thereby protecting against neural tube defects (Branda & Eaton, 1978). Melanocytes are involved in phagocytosis and melanosomes have lysosomal function (Burkhart & Burkhart, 2005), both roles contributing to immune defense. Conversely, melanin prevents the photoproduction of vitamin D, potentially leading to defective bone mineralization (Murray, 1934).
Melanin is associated with suntanning, which is currently fashionable in Western, Caucasian populations (Melia & Bulman, 1995). Conversely, among black South Africans, the use of skin lightening products is widespread, especially for upwardly mobile, educated women. Light-skinned individuals are perceived as more desirable, affluent, attractive and trustworthy than darker skinned individuals (see Glenn, 2008). If the fashionable tanning hypothesis explains preferences for skin b* coloration, melanin color should be increased more than carotenoid coloration in Caucasian faces. In the cross-cultural study, the fashionable tanning hypothesis predicts that Caucasian participants will increase skin b* values and reduce skin L* values, simulating an increase in skin melanin, while African participants are predicted to increase L* and decrease b* in African faces, simulating a decrease in skin melanin.
Section snippets
Study 1: Cross-cultural perceptions of skin color
We investigated the cross-cultural consistency of L* and b* preferences in a UK-based Caucasian population and a black South African population. We allowed black South African participants to manipulate black South African faces along skin lightness (L*) and yellowness (b*) axes simultaneously to enhance the apparent health of the faces. We compared the results to UK-based Caucasian participants' responses to a similar study using UK Caucasian faces (Stephen, Law Smith, et al., 2009).
Study 2: skin color and carotenoids in natural and supplemented diets
Study 1 showed that judgments of a healthy skin color were consistent with raised levels of carotenoid pigments. Indeed, variation in skin color within a population could reflect individual differences in intake of carotenoids from diet. We sought to establish this carotenoid–skin color relationship by (a) comparing skin color to natural dietary consumption of carotenoids, (b) using a spectral analysis to determine the specific skin pigments associated with any relationship between skin color
Study 3: Perception of carotenoid and melanin skin pigmentation
We examined the effects of skin carotenoid and melanin (the main pigments that contribute to skin b* values; Alaluf et al., 2002, Stamatas et al., 2004) coloration on perceived health. Caucasian participants were asked to manipulate the skin color of color-calibrated Caucasian facial images along empirically measured carotenoid (Fig. 4A) and melanin (Fig. 4C) color axes to “make the face as healthy as possible”. Trials were performed that allowed participants to adjust each pigment color axis
General discussion
Study 1 established a similar influence of increased skin L* and b* on perceived health in black South African and Caucasian UK-based populations, suggesting that similar preferences for skin melanin and carotenoid coloration may be predicted in both populations. Study 2 established a link between carotenoid intake (both naturally in the diet and supplemented) and skin yellowness (b*) in a Caucasian population. Study 3 established that Caucasian participants choose to increase empirically
Acknowledgments
We thank P. Hibbard, A. Hurlburt, Y. Ling, I. Penton-Voak, T. Troscianko, P. Wilcox, B. Tiddeman, M. Stirrat, J. Schindelin, D. Xiao, L. Ferrier for assistance; M. Anderson, R. Byrne, R. Caldara, P. Ferretti, T. Fitch, P. Hancock, B. Jones, M. Johnston, D. Johnston, J. Lawson, J. Seddon, R. Sprengelmeyer, M. Tovée, D. Vishnawath, D. Fessler and two anonymous reviewers for comments.
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Support: This study was supported by BBSRC, Unilever Research, ESRC, British Academy and the Wolfson Foundation.
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Competing financial interests: None of the authors have any competing financial interests.