Variation and signatures of selection on the human face

Variation and signatures of selection on the human face. [Open access]

J Hum Evol. 2014 Oct;75:143-52

Authors: Guo J, Tan J, Yang Y, Zhou H, Hu S, Hashan A, Bahaxar N, Xu S, Weaver TD, Jin L, Stoneking M, Tang K

Abstract

There has been much debate about why humans throughout the world differ in facial form. Previous studies of human skull morphology found levels of among-population differentiation that were comparable to those of neutral genetic markers, suggesting that genetic drift (neutral processes) played an important role in influencing facial differentiation. However, variation in soft-tissue morphology has not been studied in detail. In this study, we analyzed high-resolution 3D images of soft-tissue facial form in four Eurasian populations: Han Chinese, Tibetans, Uyghur and Europeans. A novel method was used to establish a high-density alignment across all of the faces, allowing facial diversity to be examined at an unprecedented resolution. These data exhibit signatures of population structure and history. However, among-population differentiation was higher for soft-tissue facial form than for genome-wide genetic loci, and high-resolution analyses reveal that the nose, brow area and cheekbones exhibit particularly strong signals of differentiation (Qst estimates: 0.3-0.8) between Europeans and Han Chinese. Our results suggest that local adaptation and/or sexual selection have been important in shaping human soft-tissue facial morphology. [. . .]

The Qpc values found in the nose and brow area between Europeans and Han Chinese approach the high differentiation reported for skin pigmentation (Relethford, 2004b). This suggests that strong local adaptation may have shaped these facial features (Myles et al., 2007). For the nose, strong correlations have been found between the nasal index and temperature/humidity, supporting climate adaptation as the major selective force (Thomson and Buxton, 1923, Davies, 1932, Weiner, 1954, Wolpoff, 1968, Hiernaux and Froment, 1976, Crognier, 1981 and Franciscus and Long, 1991). Models simulating airflow dynamics demonstrated that bigger nasal volumes, narrower shapes and downwardly pointing nares might enhance the airflow exposure of the mucosa and thereby facilitate the heating and humidification of the air (Churchill et al., 2004). The European nose shape thus may have resulted from adaptation to a colder climate. The relatively enlarged brow area in Europeans has also been noted previously (Russell et al., 1985). It has been argued that brow area size is positively correlated with the magnitude of the mechanical stresses resulting from mastication, so brow area shape differentiation (SOM, Fig. S11) could be the result of dietary differences (Russell et al., 1985). Adaptation to specific diets (Hubbe et al., 2009) and climate adaptation (Coon et al., 1950) have been hypothesized to explain the expanded zygomatics in Asians.

In addition to natural selection, sexual selection may also have played a major role in shaping interpopulation variation in the human face. Selective mate choice based on facial appearance in humans is well documented as a universal condition in global populations (Wells et al., 2009). However, whether and to what extent sexual selection shaped human facial morphology has rarely been investigated. Fisher's runaway sexual selection model suggests that a positive feedback loop composed of an arbitrary trait involving appearance, and the accidental preference of this trait in the opposite sex, could initiate a powerful sexual selection process (Fisher, 1958). It is therefore possible that some of the strong differentiation signals involving the soft-tissue facial form may have resulted from sexual selection. Further studies that combine high-resolution 3D face analysis, studies of human behavior, and genetic analyses are necessary to delineate the possible roles of local adaptation versus sexual selection in explaining the relatively large between-population differentiation that we find for soft-tissues of the human face.

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