Population affinity and variation of sexual dimorphism in three-dimensional facial forms: comparisons between Turkish and Japanese populations. Chihiro Tanikawa, M. Okan Akcam, Hatice Gokalp, Edlira Zere & Kenji Takada. Scientific Reports volume 11, Article number: 16634. Aug 17 2021. https://www.nature.com/articles/s41598-021-96029-9
Abstract: Examining the extent to which sex differences in three-dimensional (3D) facial soft tissue configurations are similar across diverse populations could suggest the source of the indirect evolutionary benefits of facial sexual dimorphism traits. To explore this idea, we selected two geographically distinct populations. Three-dimensional model faces were derived from 272 Turkish and Japanese men and women; their facial morphologies were evaluated using landmark and surface-based analyses. We found four common facial features related to sexual dimorphism. Both Turkish and Japanese females had a shorter lower face height, a flatter forehead, greater sagittal cheek protrusion in the infraorbital region but less prominence of the cheek in the parotid-masseteric region, and an antero-posteriorly smaller nose when compared with their male counterparts. The results indicated the possible phylogenetic contribution of the masticatory organ function and morphogenesis on sexual dimorphism of the human face in addition to previously reported biological and psychological characteristics, including sexual maturity, reproductive potential, mating success, general health, immune response, age, and personality.
Discussion
In the present study, principal components that explained 66.2% of the sample’s variance showed interaction between population affinity and sex were not significant, which indicates that both populations have statistically similar expressions of sexual dimorphism. Alternatively, our detailed analysis revealed that both population affinity characteristics of facial sexual dimorphism that were common to both the Japanese and Turkish subjects, and some characteristics that were unique to each set of subjects. The presence of both similarities and differences in facial sexual dimorphism among populations described in this study were consistent with previous controversial studies regarding population affinity9,10,11,12. The common characteristics could have arisen from a strong selective force on fundamental function to survive as a result of natural selection, and the differing sexually dimorphic characteristics could be due to environmental adaptation under a trade-off between natural and sexual selection22.
Regarding the common sexual dimorphic characteristics, both the Japanese and Turkish females had a shorter face height, especially with regard to the lower face; a flatter forehead; greater sagittal cheek protrusion in the posterior part of the infraorbital region; and less prominence of the cheek in the parotid-masseteric region. Furthermore, females in both population groups had antero-posteriorly smaller noses and greater retrusion of the columella base and subnasal region.
Males showed a greater height in the lower anterior face, especially with regard to the chin, in both population groups. It should be noted that a previous cephalometric study23 documented temporal changes in the ratios of the anterior lower face height to the total face height in the Japanese population. Females exhibited the anterior lower face height to total face height ratio almost equal to or longer than males at 6, 8, and 10 years old. Females at 6, 10, and 14 years old had lower face height ratios that were similar to those of adults (6 years old = 54.6% and adults = 54.9%). It is after 12 years of age when males begin to have increased face height ratio23. The observed increase in the lower anterior face height in males can be ascribed to sexual differences in pubertal growth potential of the mandible23, which is prolonged in males compared with females. There are several explanations regarding why men have a greater lower anterior face height, especially in the chin after pubertal growth. From the perspective of mastication, it seems likely that the acquired basic skill for most fundamental motor performance, such as mastication and locomotion, is independent of sex24. A previous study25 documented that the smoothness or skillfulness of masticatory jaw movement in terms of minimizing the jerk cost is not sex-specific. It should, however, also be noted that some parameters, such as the amount of jaw opening and movement velocity, are sensitive to sex-specific differences in jaw size and masticatory muscle properties25. Adult females show longer duration and lower peak velocity in masticatory jaw movement compared with males24; this can be ascribed to adult males generating greater muscle force and faster muscle contraction26 with greater muscle volume and size of the mandible, to which the jaw-closing muscles are attached. Sex influences on maximal molar bite force and masticatory muscle thickness17. Thus, the anatomy and function of the masticatory muscles may contribute to explaining why males generally have greater faces, especially in the lower third.
Furthermore, the allometric decomposition findings concerning sexual shape dimorphism support the phylogenetic importance of the chewing apparatus in sexual dimorphism in males. As men require more calories than women to function16, it is reasonable that their greater body size tends to correlate with a greater anterior facial height for a well-developed chewing apparatus. A previous study that examined 2D allometric and non-allometric variation in the facial shape differences between men and women showed a rather weak link with allometric variation compared with non-allometric variation in most populations, including the Turkish. As our study showed that the allometric difference was greater than non-allometric differences, this is considered to be related to the sex differences in the antero-posterior direction.
From a biological perspective, sex hormones are major factors related to sexual dimorphism. In males, higher androgen serum levels at puberty exert potent osteoanabolic effects and therefore may contribute to this skeletal sexual dimorphism. Animal experiments with anabolic steroids demonstrated a clear effect on craniofacial growth, mainly as an increase in total skull length and increase in the depth of the antegonial notch27. Interestingly, a previous study showed that mandibular and cortical human osteoblastic cells of both sexes expressed higher androgen receptor mRNA levels and significantly more androgen binding sites per cell and exhibited significantly greater mitogenic responses to the androgen dihydrotestosterone28. Those results indicate that the vertically greater mandibular height in males observed in our study could be due to skeletal site-dependent expression of the androgen receptor in the mandible. Additionally, a previous study that examined facial morphology of 1-year-old boys and girls showed the existence of early sexual dimorphism, and prenatal testosterone exposure is thought to be related to sexually dimorphic facial morphology29. Thus, it is possible that androgens in males could contribute to facial sexual dimorphism both before and after puberty.
Previous studies on anthropoids revealed only smaller muscle strains in the supraorbital region in contrast to those in the infraorbital region or the zygomatic arch during mastication30,31. Animal studies32,33 have also revealed that circumorbital structures became greater to provide rigidity against non-masticatory forces; these studies revealed that is unlikely that masticatory muscle forces contributed to the remodeling of the supraorbital torus. On the contrary, the development of the supraorbital ridge has been viewed as an ontogenetic adaptation to masticatory forces34. In primates, masticatory-stress models have been examined using in vivo experimental data. Primates have significant temporalis attachments that extend to almost the midline of the frontal bones; bending of the brow-ridges is thought to be due to the mastication force pushing upward and the masseter and temporalis muscles pulling downward35. Few of the previous computational models, using finite element analysis of primate skulls36, agree with these in vivo findings. A previous study37 found a positive correlation between the mesio-distal crown width of the mandibular first molar and the size of the supraorbital ridge in humans. Occlusal forces exerted on the molar teeth contribute to supraorbital torus formation. Because females generate weaker muscle force and slower muscle contraction than males26, and exhibit decreased maximal molar bite force and masticatory muscle thickness17, we should not rule out the possibility of contribution of masticatory muscle forces to supraorbital ridge formation in humans. Phylogenetically, the smaller supraorbital ridge observed in the female subjects in the present study may be explained by the differences in masticatory force magnitude and its relevant jaw muscle thickness between males and females17,30.
In the present study, both Japanese and Turkish males showed an antero-posteriorly greater nose when the eye distances were standardized. This result is in line with those of previous studies38,39,40. Previous studies primarily hypothesized that males have evolved to have greater nasal cavity dimensions to facilitate the oxygen intake that is needed to maintain a larger body mass37,41. The degree of sexual dimorphism in nasal shape is considered to be potentially due to the functional integration between the nasal cavity and the respiratory system42.
The extent of the cheek region is defined as “superiorly to the zygomatic arch, inferiorly to the margin of the mandible, posteriorly to the ear, and anteriorly to the corner of the mouth” and is divided into four parts as topographical regions: infra-orbital, buccal, zygomatic, and parotid–masseteric regions43).
In the present study, in the infraorbital and buccal regions, the sagittal cheek protrusion in the posterior part of the infraorbital region was greater in the female subjects on the left side. Furthermore, lesser prominence of the cheek in the parotid–masseteric region was also observed in both Japanese and Turkish female subjects.
A lesser prominence of the cheek in the parotid–masseteric region can be explained by the smaller masseter muscles in women17. Thin masseter muscles lead to a lesser prominence of the cheek in the parotid–masseteric region in women.
Effects of developmental and functional interactions on morphological variability of the head through ontogeny have been discussed in previous studies42,44. Several studies42,44 have claimed that genetic signals determine the initial geometry of craniofacial anatomy, and that geometry is altered by the local mechanical environment, such as masticatory function and respiratory function, through variations in the spatio-temporal interplay of depository and resorptive activity of bone. In contrast, there is very little concrete evidence of the relationship between functional and phylogenetic development in facial configurations. In general, it is assumed that varying environmental conditions, such as climates, geographic areas, and dietary resources, require physical characteristics, including dento-facial features, which contribute to maximizing the survival probability of individuals. Hominids are now recognized as showing higher adaptability to their surrounding environment based on related morphological changes than was previously understood.
In the past, several studies have addressed 3D morphological differences between populations. For example, between Caucasians and African-Americans, the most distinct differences were observed in the forehead, alar base, and perioricular regions using 3D facial data45; between Caucasians and Asians, differences were observed in the malar and zygomatic areas, forehead, lips, and chin46. Even in the phylogenetically related populations, there were differences seen in the nasal, malar, lips, and lower facial regions between two population groups (Budapest, Hungary, and Houston, Tex)47; differences were also observed in the nasal width, eye distances, and facial height of two European Caucasian populations of close phylogenetic and geographic proximity (UK and Netherlands)14. In short, the previous studies described the facial differences between the population groups; however, limited data has been reported regarding varied facial sexual dimorphic characteristics among populations.
In the present study, four features in the Japanese and three in the Turkish were found to be exclusive sexual dimorphic characteristics. In the Japanese subjects, females had greater eye height (i.e., brighter eyes) compared with males. A medium or high upper eyelid crease is known to represent an attractive face in East Asian females, and 50% of females exhibit a minimal or absence of a double eyelid44. Although greater eye height is also deemed an important factor for facial attractiveness in other populations, the present results indicate that eye height is a visible facial sexual dimorphism that is more discriminatory in the Japanese subjects than the Turkish subjects.
Japanese females also showed a smaller anteroposterior protrusion of the nasal dorsum at the orbital level (i.e., a flatter nose) and a superiorly positioned mouth with a vertically shorter subnasal region. Additionally, shorter horizontal mandibular width was observed in the Japanese females. These findings indicate that Japanese females had overall smaller middle and lower facial structures than males. In a previous study that examined the 3D nasal shape and genotype in 3746 individuals, nares width was correlated with temperature and absolute humidity48. This result indicates that at least sexual dimorphism in nasal shape may change because of climate adaptation.
In contrast to the Japanese females, three features were found to be characteristic of the Turkish females compared with Turkish males. There was a greater vertical distance between the eyes and eyebrows, and an increased zygomatic width compared with exocanthion–exocanthion distance. These traits reflect a stout upper facial structure. Facial ontogeny research on immature hominids with a finite element model49 showed that bone deposition was identified over the outer aspects of the orbits, lateral nasal walls, infraorbital region, zygomatico-maxillary region, parts of the mid-clivus, including the canine jugum, and interincisal protuberance, as well as portions of the nasal sill and areas lateral to the intermaxillary suture; they inferred that these changes were related to the masticatory system49.
A shallower labio-mental sulcus also characterized Turkish female compared with male faces. A recent study39 indicated that an ontogenetic decrease in chin prominence was associated with increased vertical bending resistance and vice versa. Thus, it can be inferred that a shallow labiomental sulcus was unique to the current Turkish female participants, which indicates an adaptational response of Turkish females, who have delicately constituted jaw bones and muscles, compared with Turkish males in a dietary environment that includes tougher animal proteins compared with the Japanese dietary environment.
It is well known that Africa is the ancestral homeland of modern humans50. A phylogenetic tree showed the categorization of the world population into nine sub-populations based on the polymorphisms of protein genes of 1915 populations: African; North African and West Asian; European; Amerind; Arctic Northeast Asian; Northeast Asian; Southeast Asian; Pacific Islander; and New Guinean and Australian51. The genetic distances between Japanese (Northeast Asian) and Turkish (European) were moderately far (55% of total distance) whereas European and North African were close (7%); this indicated that Japanese and Turkish (European) had different developmental route51. Genetic data also provided some indication that the spread of humans into Asia was along the coast to south and south-east Asia, from where it bifurcated to the north and south52. Thus, our comparisons of sexual dimorphism in facial forms between Turkish and Japanese populations can explain a relatively long span of genetic drift, which is the result of population variation among individual genotypes in their probabilities of survival and/or reproduction.
Several limitations associated with the present study warrant mention. First, the Turkish population was undersampled in comparison to the Japanese population. The frontal view of our 3D Turkish data was similar to that of a previous 2D study53 which used a greater number of Turkish samples (n = 264); thus it could be said that our results are possibly representative of the Turkish population. However, future studies including more Turkish subjects would us to make more general conclusions. Second, our study included only two populations, so it is impossible to draw complex conclusions regarding the geographical variability of the human face. Future studies would benefit from including an even larger number of populations. Third, in the present study, we used only the centroid size of the face to examine the allometric component. The results may vary when using the height or weight. Furthermore, in the present study, we omitted color information when analyzing the data because this information was not stable among populations. In some populations, not only sexual dimorphism in facial shape but also sex differences in skin color contribute to the overall facial dimorphism. Furthermore, it has been shown that skin color is an important trait associated with facial attractiveness in populations showing high variation in skin color, especially in Africans54,55. This means that facial dimorphism cannot be considered only by the facial shape, and there is still a place for sexual selection that may act upon non-shape-associated facial traits. Moreover, it seems that some color traits (such as iris color) are systematically associated with the sex-specific facial shape56,57. Future studies using information involving sex differences in these other attributes rather than shape should be considered. Finally, although the present study does not provide a convincing explanation about whether the sexual dimorphisms, which were determined in the present study to be unique to each population group, represent consequences of natural selection for population affinity that successfully adapted to dietary environments for many generations. Therefore, although we must be cautious about the limitations of interpreting these data, the results of the present study further enhance our understanding of human sexual dimorphism expressed in the oral and facial regions.
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