Original article
Facial sexual dimorphism, developmental stability, and susceptibility to disease in men and women

https://doi.org/10.1016/j.evolhumbehav.2005.06.001Get rights and content

Abstract

We investigated aspects of self-reported health history–the number and duration of respiratory and stomach or intestinal infections and the number of uses of antibiotics over the last 3 years–in relation to measured facial masculinity, developmental instability [facial asymmetry and body fluctuating asymmetry (FA)] and facial attractiveness in a sample of 203 men and 203 women. As predicted from the hypothesis that the degree of facial masculinity is an honest signal of individual quality, men's facial masculinity correlated negatively and women's positively with respiratory disease number and duration. Stomach illness, however, was not associated significantly with facial masculinity and antibiotic use correlated significantly (negatively) only with men's facial masculinity. For both facial asymmetry and body FA, significant, positive associations were seen with the number of respiratory infections. In addition, facial asymmetry was associated positively with the number of days infected and marginally, in the same direction, with antibiotic use. Facial attractiveness showed no significant relationships with any of our health-history measures. This study provides some evidence that facial masculinity in both sexes may signal disease resistance and that developmental stability covaries positively with disease resistance. The validity of our health measures is discussed.

Introduction

On average, many of men's and women's facial structures differ. Men have broader and longer chins, deeper and narrower eyes due to brow ridge development, and thinner lips. Sexual dimorphism is facilitated ontogenetically by the ratio of testosterone to estrogen during adolescence (Bardin & Catterall, 1981, Enlow, 1990; see also references in Swaddle & Reierson, 2002). In men, a high ratio influences facial growth until the early 20s (Enlow, 1990). Possibly, estrogen caps the growth of the facial bones, as it does for some other bones, but enhances lip fullness, whereas testosterone, in combination with growth hormones, promotes facial bone growth (for further discussion, see Thornhill & Gangestad, 1993, Thornhill & Grammer, 1999). Sexually dimorphic facial structure hereafter is referred to as “facial masculinity.”

Facial masculinity has been a focus of studies of sexual selection in humans. Men with masculine faces may tend to be socially dominant (Mazur & Booth, 1998, Mueller & Mazur, 1997, Swaddle & Reierson, 2002), and hence, men's facial masculinity may play a role in male intrasexual selection. It also affects female choice. The face that normally ovulating women (not using hormone-based contraception) who are at the fertile phase of their ovulatory cycle find most attractive is more masculine than the face found most attractive by women during other phases of the cycle (Johnston et al., 2001, Penton-Voak & Perrett, 2000, Penton-Voak et al., 1999). One report found this to be especially true when these women are pair-bonded and rating faces for short-term sexual relationships (Penton-Voak et al., 1999). Female preference for men's facial masculinity primarily at peak fertility in the ovulatory cycle, the absence of the preference in women not ovulating due to hormonal contraception, and an enhanced preference in pair-bonded women seeking short-term sexual relationships suggest that the preference is an adaptation that functions to obtain for the offspring a sire of superior genetic quality (Johnston et al., 2001, Penton-Voak & Perrett, 2000, Penton-Voak et al., 1999).

That men's facial masculinity may be involved in intrasexual competition and intersexual selection suggests that facial masculinity honestly signals individual phenotypic and related genetic quality (Grammer & Thornhill, 1994, Mueller & Mazur, 1997, Thornhill & Gangestad, 1993). Honest signaling here might work through an immunocompetence handicap mechanism (Folstad & Karter, 1992): Testosterone compromises the immune system's ability to combat disease; hence, only men with superior immune systems can afford high testosterone levels and associated masculinization. Alternatively, high masculinity may signal quality because testosterone allocates energy to functions involved in male–male competition (e.g., muscle growth) that men lacking key competitive abilities do not benefit from to the same extent (McDade, 2005, Thornhill & Gangestad, 1999a, Thornhill & Gangestad, 1999b). In any case, honest signaling through facial masculinization may be partly mediated socially through ongoing male–male competitive testing of quality. (See Roberts, Buchanan, & Evans, 2004, for a review of alternative honest-signal hypotheses and Zahavi & Zahavi, 1997, for further discussion of honest signal evolution).

Fitness is an individual's design for reproductive success, not merely reproductive success (Williams, 1966). Reproductive success arises, in part, through stochastic processes rather than the design of an individual's traits for solving problems affecting differential reproductive success of individuals. The truth in an individual's honest signal, that is, the phenotypic and genetic quality that the signal depicts, corresponds to the individual's fitness. The evidence reviewed above suggests that men's masculinity contains information about their breeding values for producing sons who will be successful in competition for mates at the fertile phase of their cycle.

But does men's masculinity honestly signal breeding value for fitness components other than mating success? Relationships between sexually selected traits and fitness components other than mating success are of major theoretical interest. The Darwinian–Fisherian theory of sexual selection's operation proposes that sexual selection favors traits that enhance the mating success of offspring solely through their increased sexual attractiveness. In this case, sexual selection results in increased frequencies of alleles that cause, through the ontogenetic process, the production of offspring that possess enhanced reproductive value, but only in terms of sexual attractiveness and, hence, mating success. Other theories of sexual selection propose that sexual selection favors sexual attractiveness because it is defined by its covariation with other fitness components (Andersson, 1994, Kokko et al., 2002). In terms of men's masculinity, the question is whether masculinity affects mating success alone or is associated with mating success as well as additional fitness components.

As Kokko et al. (2002) point out, the Darwinian–Fisherian model need not (indeed, should not) imply that, when male sexually selected features covary only with attractiveness, they are not indicators of individual phenotypic and genetic quality. Quality reflects an organism's capacity to generate fitness-enhancing outcomes. Although, under natural conditions, quality should be associated with fitness and generally reproductive success, it need not covary positively with all fitness components, including longevity and health. In some circumstances, selection can favor such extreme investment in sexually selected indicators by high-quality males that they actually have higher rates of mortality and morbidity than do lower quality males (see also Getty, 2002). Empirically, across many species, more ornamented males, compared with less ornamented males, have reduced parasitism and stronger immunity (Møller, Christie, & Lux, 1999) and increased adult survival (Jennions, Møller, & Petrie, 2001), although these patterns are by no means universal across studied species. In a species such as humans, we should probably not expect sexual selection to be sufficiently strong to drive covariation between sexually selected phenotypic indicators of quality and fitness components other than mating success to be negative (although these associations may be weak).

Studies involving multiple approaches have examined the covariation of men's facial masculinity and fitness components other than mating success. One approach examines the associations between rated masculinity of men's facial pictures and rated health of the same faces or actual health history of the men based on medical records. Rhodes, Chan, Zebrowitz, and Simmons (2003) reported that rated masculinity in adolescent male faces correlates positively with rated and actual health (see also Zebrowitz & Rhodes, 2004). Another approach examines health associations using measured facial masculinity based on facial traits showing sexual dimorphism. Gangestad and Thornhill (2003) reported that measured facial masculinity correlates positively with developmental stability, a component of developmental health. Developmental instability was estimated by measuring body (as fluctuating asymmetry, FA) and facial asymmetry, both of which negatively correlated with men's facial masculinity. Men's facial asymmetry also showed a curvilinear association: Highly feminine and highly masculine male faces were more asymmetric. Gangestad and Thornhill found no evidence that women's facial masculinity linearly relates to body FA but did find a significant curvilinear relationship similar to that found in men. By contrast, Koehler, Simmons, Rhodes, and Peters (2004) found no evidence for associations between body FA or face symmetry and men's measured facial masculinity. In women, they found little evidence that facial asymmetry is associated with masculinity, although body FA positively predicted facial masculinity.

In the current study, we explored further the associations between facial masculinity and health, specifically, associations with incidence of diseases that we assume are parasitic. Ancestrally, individuals' defense against parasitic infections may have been an important fitness component. Through questionnaire, we asked university students to report the number and duration of respiratory and stomach or intestinal influenza infections and antibiotic use over the last 3 years. We examined associations with facial masculinity, measures of developmental instability, and facial attractiveness.

We predicted that men's facial masculinity covaries negatively with these health measures and that women's facial masculinity covaries positively with them. Positive relationships in women are predicted because high masculinity in women corresponds to low estrogen levels. It has been proposed that femininity (facial and bodily estrogenization) signals individual quality in women (Singh, 1993, Singh, 1995, Thornhill & Gangestad, 1993, Thornhill & Grammer, 1999).

We predicted the negative associations between health measures and body and facial FA. In many species, including humans, developmental stability appears to be associated positively with health (Møller & Swaddle, 1997, Thornhill & Møller, 1997, Waynforth, 1998). Jones et al. (2001) and Rhodes et al. (2001) found that symmetric faces are rated as healthier than are asymmetric faces, but no consistent relationship between facial symmetry and actual health based on health records.

We predicted a positive association between health and female facial attractiveness but offered no prediction for men's attractiveness. Although some evidence suggests that facial attractiveness predicts health, results are mixed. Meta-analyses found a positive relationship between facial attractiveness and mental (Feingold, 1992, Langlois et al., 2000) and physical health (Langlois et al., 2000; but see Kalick, Zebrowitz, Langlois, & Johnson, 1998). Robust associations between women's facial attractiveness and facial femininity (e.g., Penton-Voak, Jacobson, & Trivers, 2004) suggest associations between the former and health measures. Men's attractiveness, however, does not consistently covary with masculinity. Penton-Voak et al. (2004) found a greater female preference for masculinity in men's faces in Jamaica than in the U.K. They argue that male facial attractiveness reflects assessment of paternal investment qualities as well as genetic quality. In societies in which women place particular importance on investment qualities (e.g., U.K.), feminine male faces may be more attractive than masculine ones. Where women find male facial masculinity most attractive, they presumably place greater value on genetic quality.

Section snippets

Methods

The data are derived from our larger study of 406 students (203 men and 203 women) at The University of New Mexico on developmental instability and romantic relationships (see Gangestad & Thornhill, 1997, for a fuller description of the sample). Of these, 295 participants provided the results reported by Gangestad and Thornhill (2003).

Results

Analyses were performed using GLM (SPSS-PC 12.0). The results for associations between developmental instability and masculinity in the men and women are reported in Gangestad and Thornhill (2003). The current paper focuses on facial masculinity and developmental stability in relation to the health measures.

For each predictor–facial masculinity, body FA, facial FA, and physical attractiveness–three sets of initial GLM analyses were performed. First, we performed analyses on number of

Discussion

The current research asked young men and women to self-report their respiratory and intestinal/stomach infections, total duration of each type of infection, and antibiotic use over the last 3 years. Based on theory and data concerning the evolution of sexually selected traits, we predicted that men's reports would negatively covary with facial masculinity, and women's reports would show positive relationships. Overall, the results supported the prediction: There was a significant interaction

Acknowledgments

Preparation of this report was supported partially by the National Science Foundation Grant Award 0136023. We thank Ruth Mace and two anonymous reviewers for criticisms that improved the paper.

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