Human Facial Shape and Size Heritability and Genetic Correlations

Abstract

The human face is an array of variable physical features that together make each of us unique and distinguishable. Striking familial facial similarities underscore a genetic component, but little is known of the genes that underlie facial shape differences. Numerous studies have estimated facial shape heritability using various methods. Here, we used advanced three-dimensional imaging technology and quantitative human genetics analysis to estimate narrow-sense heritability, heritability explained by common genetic variation, and pairwise genetic correlations of 38 measures of facial shape and size in normal African Bantu children from Tanzania. Specifically, we fit a linear mixed model of genetic relatedness between close and distant relatives to jointly estimate variance components that correspond to heritability explained by genome-wide common genetic variation and variance explained by uncaptured genetic variation, the sum representing total narrow-sense heritability. Our significant estimates for narrow-sense heritability of specific facial traits range from 28 to 67%, with horizontal measures being slightly more heritable than vertical or depth measures. Furthermore, for over half of facial traits, >90% of narrow-sense heritability can be explained by common genetic variation. We also find high absolute genetic correlation between most traits, indicating large overlap in underlying genetic loci. Not surprisingly, traits measured in the same physical orientation (i.e., both horizontal or both vertical) have high positive genetic correlations, whereas traits in opposite orientations have high negative correlations. The complex genetic architecture of facial shape informs our understanding of the intricate relationships among different facial features as well as overall facial development.

Keywords: complex traits; facial shape; facial size; heritability; morphometrics.

Figure 1

3D facial scan with annotated landmarks. Landmarks annotated are defined in Table S1.

Figure 2

Study age distribution by sex.

Figure 3

Heritability of 38 facial traits. The bar plot represents h²_g (yellow), missing h² (blue), and total h² (yellow + blue) with error bars for all 38 facial phenotypes analyzed. Bars that apparently have no missing h² (blue) indicate that h²_g equals h²; therefore, narrow-sense heritability of that phenotype can be explained fully by common genetic variation.

Figure 4

Heritability of linear distances by measurement orientation. The bar plot represents h²_g (yellow), missing h² (blue), and total h² (yellow + blue) with error bars for 25 linear distances. Traits are first clustered by orientation, then by facial structure with between-trait phenotypic correlations seen in the colored matrix in the bottom half of the figure.

Figure 5

Distribution of variance components across the face. (A–C) The anatomical distribution of phenotypic and genetic variances as well as heritabilities is shown. These are represented as heatmaps based on a thin-plate-spine morph as described in Materials and Methods. (D) The heritability estimates or the Procrustes-superimposed symmetrized landmarks are shown. (E) The vectors, magnified 10-fold, used to generate the heritability heatmap are depicted.

Figure 6

Pairwise genetic correlation matrix of the linear distances. Genetic correlation was calculated from >15 million common genetic variants. Traits that have high positive genetic correlations with each other are shown in blue, indicating that the same genetic loci alter the magnitude of those traits in the same direction. Traits that have high negative genetic correlations with each other are shown in red, indicating that the same genetic loci are contributing to each phenotype in opposite directions, increasing one while decreasing the other. Genetic correlation estimates that are significantly different (P < 0.05) from 0 to +1 or 0 to −1 are marked with ○ and genetic correlation estimates that are significantly different (P < 0.05) than 0, +1, and −1 are marked with ○.