Significance Facial masculinity has been considered a sexual ornament in humans, akin to peacock trains and stag antlers. Recently, studies have questioned the once-popular view that facial masculinity is a condition-dependent male ornament signaling immunocompetence (the immunocompetence handicap hypothesis). We sought to rigorously test these ideas using high-resolution phenotypic (3D facial images) and genetic data in the largest sample to date. We found no support for the immunocompetence handicap hypothesis of facial masculinity in humans. Our findings add to a growing body of evidence challenging a popular viewpoint in the field and highlight the need for a deeper understanding of the genetic and environmental factors underlying variation in facial masculinity and human sexual dimorphism more broadly.

Abstract Recent studies have called into question the idea that facial masculinity is a condition-dependent male ornament that indicates immunocompetence in humans. We add to this growing body of research by calculating an objective measure of facial masculinity/femininity using 3D images in a large sample (n = 1,233) of people of European ancestry. We show that facial masculinity is positively correlated with adult height in both males and females. However, facial masculinity scales with growth similarly in males and females, suggesting that facial masculinity is not exclusively a male ornament, as male ornaments are typically more sensitive to growth in males compared with females. Additionally, we measured immunocompetence via heterozygosity at the major histocompatibility complex (MHC), a widely-used genetic marker of immunity. We show that, while height is positively correlated with MHC heterozygosity, facial masculinity is not. Thus, facial masculinity does not reflect immunocompetence measured by MHC heterozygosity in humans. Overall, we find no support for the idea that facial masculinity is a condition-dependent male ornament that has evolved to indicate immunocompetence.

The condition-dependent hypothesis is used to explain the evolution of male ornaments in nonhuman animals (1⇓⇓⇓–5). According to this hypothesis, male ornaments (e.g., reindeer antlers and peacock trains), which grow to exaggerated proportions even though they might be detrimental to fitness (6, 7), are adaptations signaling the underlying physiological and genetic quality of the individual to females. Such traits are more sensitive to the overall growth of individuals and more variable than other traits (8⇓⇓⇓⇓⇓–14). As growth itself is dependent on a variety of genetic and environmental factors, including immunocompetence, inbreeding, health status, and nutrient availability (15⇓⇓⇓–19), slight variations in physiological and genetic quality among males are amplified to perceptible levels in sexual ornaments, making them reliable indicators of underlying health (8, 9, 13). The condition-dependent hypothesis has also been applied to humans to explain the evolution of secondary sexual characteristics, such as facial masculinity and deep voices (20⇓⇓⇓–24). The apparent attraction of women to these traits, which appears to be heritable (25), is thought to be an evolutionary adaptation that helps women secure direct (e.g., investment of a healthy male) and indirect (e.g., “good genes” for their children) benefits (1, 3, 26, 27).

Among all of the factors placed under the umbrella of “condition,” immunocompetence has received considerable attention. This is, in part, because of the supposed immunosuppressive effects of androgens (28, 29), which are involved in the development of secondary sexual traits in males (22). According to the immunocompetence handicap hypothesis (ICHH), androgens mediate the allocation of resources between the competing demands of fighting infections and the development of energetically “costly” sexual ornaments (30⇓⇓⇓⇓⇓⇓⇓⇓⇓⇓–41). Consequently, males with more effective immune systems may withstand higher androgen levels, and the accompanying immunosuppressive burden, and can “afford” more extravagant displays. If this were true, then secondary sexual characteristics could serve as reliable (“honest”) indicators of the physiological and immunological quality of males (7, 35, 40, 42). Parts of the ICHH have found some support in humans (36, 43⇓–45) and nonhuman animals [for review, see Roberts et al. (46)].

However, the evidence linking secondary sexual traits to the condition, immunological or otherwise, of human males is ambiguous and inconsistent across studies (44, 46⇓–48). That androgens are immunosuppressive also does not appear to be well-supported (49). This has recently led many to question the applicability of the ICHH in humans, particularly with respect to facial masculinity (49⇓–51). Some of the inconsistency has been attributed to methodological limitations, such as small sample size and the use of measures of perceived masculinity and attractiveness, which are influenced by sociocultural factors that are difficult to control in observational studies (50). Another limitation that has received less attention is the lack of correction for ancestry and population structure, which can lead to spurious associations. Because of these issues, a rigorous study of the link between facial masculinity and immunocompetence and/or condition is needed.

In this study, we investigated the condition-dependent hypothesis and ICHH in humans with respect to facial masculinity. Working from theory and evidence from research on condition dependence of sexual ornaments in nonhuman animals (1⇓⇓⇓–5, 8), we tested three hypotheses:

Hypothesis 1: Facial masculinity is a condition-dependent male ornament in humans. If this is true, then we expect facial masculinity to be (i) more strongly correlated with overall growth in males relative to females, and (ii) more variable in males compared with females.

Hypothesis 2: Immunocompetence is associated with overall growth in humans. If immunocompetence plays a role in condition-dependent expression of secondary sexual characteristics, then it should be correlated with overall growth in humans.

Hypothesis 3: Facial masculinity reflects immunocompetence in men. Males who show greater immunocompetence should exhibit more masculine faces than males with lower immunocompetence. In contrast, facial masculinity should be less sensitive to variation in immunocompetence in females.

To test our hypotheses, we used an objective measure of facial masculinity, calculated with high resolution 3D photographs in a large sample of persons of European ancestry. We used height as a proxy for overall growth and condition as height is known to be associated with health, income, nutrition, and exposure to disease and infection (15⇓–17). We used individual heterozygosity at the major histocompatibility locus (MHC) as a measure of immunocompetence. The MHC locus, also known in humans as the HLA complex, is located on chromosome 6 and contains around 200 genes that are involved in immune function (52). Higher genetic diversity at the MHC enables the immune system to recognize a more diverse array of foreign antigens (52⇓–54). As a result, the MHC has experienced balancing selection in both humans and nonhumans (52, 55⇓⇓–58). Therefore, heterozygosity at this locus serves as a useful proxy to measure immunocompetence. Finally, we considered the effects of body size on facial masculinity (allometry) in addition to other likely confounders, such as age, weight, genome-wide heterozygosity, and population structure.

Discussion Condition-dependent male ornaments tend to be highly variable and more sensitive to variation in growth among males (i.e., exhibit greater allometric effects in males compared with females) (8, 10, 13, 14). Facial masculinity does not meet these expectations as neither the allometric nor the nonallometric component of facial masculinity is more variable in males compared with females, and the allometric effects of growth on facial masculinity are similar across the sexes. Because diversity at the MHC locus is important for antigen recognition and presentation and the locus is known to be under balancing selection in many species, including humans, heterozygosity at this locus is an important marker of immunocompetence. This is supported by our finding that people who are more heterozygous at the MHC locus are taller, on average, than people who are less heterozygous, suggesting that variation at the MHC locus might be important for growth. We find that facial masculinity is not significantly associated with MHC heterozygosity, either in males or females. Our results do not support the hypothesis that facial masculinity is an indicator of immunocompetence. However, we cannot rule out the effect of other measures of immunocompetence such as non-MHC genes and antibody titers. We also find no support for the contention that FM indicates heterozygosity across the genome generally, something that has also been hypothesized previously (3, 71). Altogether, our findings add to the growing number of studies questioning some of the evolutionary explanations behind female and male perceptions of facial masculinity (50, 51) and whether masculinity should be regarded as a condition-dependent male ornament in humans. Nevertheless, there are many questions related to facial sexual dimorphism and masculinity in humans that need to be addressed from an evolutionary standpoint. Humans show intermediate levels of allometric cranial sexual dimorphism among extant hominids (65), and we do not know whether this degree of sexual dimorphism is new to humans since their divergence from other hominins and apes. Did some aspects of facial masculinity evolve as a mechanism to intimidate rival males (72⇓–74), or do they represent vestigial traits that have decreased over time as a result of self-domestication (75⇓–77)? We also do not know how facial sexual dimorphism varies across human populations although we suspect that it does so considerably, both in degree and pattern, given that our results show that it varies significantly across Europe. Is genetic drift sufficient to explain these patterns? If not, can these patterns be explained by differences in perceptions of beauty and social status across populations? It is important to tackle these questions by careful comparison of the degree and pattern of sexual dimorphism within and across populations, as well as how sexual dimorphism is perceived cross-culturally. Equally important is the need to fill gaps in our knowledge of the proximate causes underlying sexual dimorphism and facial masculinity. We know that differences in facial shape exist between male and female children as young as 3 y old (66, 68, 78) and are likely defined, in part, by the intrauterine environment during gestation (79⇓–81). This dimorphism increases dramatically at the onset of puberty, implicating sex hormones and other endocrine processes underlying general growth during this period (66, 68, 82⇓⇓–85). These observations suggest that facial masculinity may arise because of extended overall growth and higher circulating androgen levels in pubertal males (66, 84, 86). However, sex differences in face shape are not merely developmental byproducts of extended overall growth in males as we and others have shown that sex has a significant effect on facial shape even after adjusting for body size (63, 65⇓⇓–68). Variation in facial masculinity also cannot be attributed solely to differences in circulating androgens during puberty. This is clear from the observation that, despite the fact that males exhibit higher mean and variance in androgen levels compared with females (87), they are not more variable in terms of facial masculinity. In fact, a recent report shows that the heritability of facial masculinity is similar between males and females, and the correlation between facial masculinity of same-sex siblings is similar to that of opposite-sex siblings (88). These results are indicative of a shared genetic architecture underlying facial masculinity in males and females and further serve to deemphasize the idea that facial masculinity is a male-specific ornament. It will be important to explore the effects of other hormones (e.g., estrogen and estradiol) and sex-chromosomal genes (89⇓–91), as well as the timing of these effects. These questions are fundamental for cultivating a more mechanistic understanding of the development of sexual dimorphism, which, in turn, will lead to a better understanding of the role of sexual selection in human evolution.

Acknowledgments We thank the participants for providing the data necessary to carry out this study. We thank the members of the M.D.S. laboratory and the D.A.P. laboratory for helping with data collection; and thank Tina Lasisi and Tomás González-Zarzar for helpful discussions on the manuscript. Finally, we thank the Penn State Center for Human Evolution and Diversity (CHED), Research Fund KU Leuven (Grant BOF-C1, C14/15/081), and the Research Program of the Fund for Scientific Research–Flanders (Belgium) (Grant FWO, G078518N) for funding.

Footnotes Author contributions: A.A.Z. and M.D.S. designed research; A.A.Z., J.D.W., B.C.M., and C.R.L. performed research; A.A.Z., J.D.W., P.C., and M.D.S. contributed new reagents/analytic tools; A.A.Z., J.D.W., and P.C. analyzed data; A.A.Z., J.D.W., D.A.P., and M.D.S. wrote the paper; A.A.Z. and J.D.W. helped with data collection; M.D.S., B.C.M., and C.R.L. organized data collection; and D.A.P. and M.D.S. supervised research.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission. L.M.D. is a guest editor invited by the Editorial Board.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1808659116/-/DCSupplemental.