Sutural growth restriction and modern human facial evolution: an experimental study in a pig model

Abstract

Facial size reduction and facial retraction are key features that distinguish modern humans from archaic Homo. In order to more fully understand the emergence of modern human craniofacial form, it is necessary to understand the underlying evolutionary basis for these defining characteristics. Although it is well established that the cranial base exerts considerable influence on the evolutionary and ontogenetic development of facial form, less emphasis has been placed on developmental factors intrinsic to the facial skeleton proper. The present analysis was designed to assess anteroposterior facial reduction in a pig model and to examine the potential role that this dynamic has played in the evolution of modern human facial form. Ten female sibship cohorts, each consisting of three individuals, were allocated to one of three groups. In the experimental group (n = 10), microplates were affixed bilaterally across the zygomaticomaxillary and frontonasomaxillary sutures at 2 months of age. The sham group (n = 10) received only screw implantation and the controls (n = 10) underwent no surgery. Following 4 months of post-surgical growth, we assessed variation in facial form using linear measurements and principal components analysis of Procrustes scaled landmarks. There were no differences between the control and sham groups; however, the experimental group exhibited a highly significant reduction in facial projection and overall size. These changes were associated with significant differences in the infraorbital region of the experimental group including the presence of an infraorbital depression and an inferiorly and coronally oriented infraorbital plane in contrast to a flat, superiorly and sagittally infraorbital plane in the control and sham groups. These altered configurations are markedly similar to important additional facial features that differentiate modern humans from archaic Homo, and suggest that facial length restriction via rigid plate fixation is a potentially useful model to assess the developmental factors that underlie changing patterns in craniofacial form associated with the emergence of modern humans.

Fig. 1

Rigid microplates affixed bilaterally across the frontonasomaxillary and zygomaxillary sutures in an experimental pig. Note that this figure is for illustrative purposes only and this pig was not included in the analysis.

Fig. 2

Cranial base angle was measured, using computed tomography scans, as the angle between the foramen cecum–sella (fc-s) and sella–basion (s-ba) lines.

Fig. 3

External 3D coordinate landmarks for cranium (A), mandible (B) and infraorbital region (C). The grid in C is a subsection of a larger scaled grid that was fitted to each pig and extended anteroposteriorly from the inferiormost aspect of the premaxillary–maxillary suture to the superiormost aspect of the zygomaticotemporal suture and superoposteriorly from the inferiormost aspect of the premaxillary–maxillary suture to the frontolacrimal suture. The smaller grid used in the geometric morphometric analysis ranged from the maxilla to the body of the zygomatic. rh, rhinion; n, nasion; b, bregma; l, lambda; ba, basion; h, hormion (located in the midsagittal plane on the sphenoid just posterior to the vomer); st, staphylion; pr, prosthion; cr, coronion; cd, condylion; go, gonion; gn, gnathion; id, infradentale; M₂, distal M₂ at the alveolus.

Fig. 4

Comparison of a representative control (A) and a representative experimental (B) pig.

Fig. 7

Scatter plot of individual PC1 scores on individual centroid values. PC1 was statistically significantly correlated with centroid size (r= 0.43; P= 0.023).

Fig. 6

Thin-plate spines illustrating variation of 3D coordinate shape variables along PC1 in the midsagittal plane. The experimental group (negative PC scores) exhibits a reduction in facial length and a reorientation of the snout relative to the neurocranium. The mandible exhibits a reorientation concomitant with the facial skeleton although it does not exhibit the same reduction in anteroposterior dimensions. Although not included in the visualization as line segments, all coordinate landmarks (i.e. infraorbital and cranial base landmarks) were included in the derivation of PC scores. Visualizations of the cranial base and infraorbital region, as line segments, were excluded from this figure to aid in the visualization of other morphological features.

Fig. 5

Scatter plot of individual principal component scores derived from the Procrustes shape variables. PC1 (32.2%) describes variation between the experimental and control/sham pigs. Variation in PC scores along PC1 was statistically significant (P < 0.001). Black circles, control/sham group; gray circles, experimental group.

Fig. 8

Thin-plate spines illustrating variation of 3D coordinate shape variables along PC1 in the midsagittal plane with the cranial base visualized. No differences in cranial base angle are evident in the splines (experimental group, negative PC scores; control/sham group, positive PC scores). Any variation in the orientation of the cranial base follows the orientation of the neurocranium as a whole. Similarly, there are no differences in the relative sizes of the anterior and posterior cranial base. Visualizations of the mandible and infraorbital region, as line segments, were excluded from this figure to aid in the visualization of other morphological features.

Fig. 10

(A) Thin-plate splines illustrating variation of 3D coordinate shape in the infraorbital region along PC1. In this figure, the splines are oriented sagittally and are located lateral to the midsagittal plane. The experimental group (negative PC scores) is characterized by an infraorbital region that faces inferiorly, whereas the infraorbital region of the control/sham group (positive PC scores) faces superiorly. This is further illustrated by the representative experimental (B) and control/sham (C) pigs. The dashed line along the infraorbital region, from the frontolacrimal suture to the zygomatic root, of the experimental pig shows the greater inferior orientation of the zygomaxillary surface. In contrast, the dashed line of the control/sham pig shows the superiorly oriented zygomaxillary surface. Visualizations of the cranial base and infraorbital region, as line segments or surface renderings, were excluded from this figure to aid in the visualization of other morphological features.

Fig. 9

(A) Thin-plate splines illustrating variation of 3D coordinate shape variables in the infraorbital region along PC1. Selected landmarks are labeled to aid visualization. In this figure, the splines are in the horizontal plane and is located approximately in the middle of the infraorbital region near the inferior margin of the orbital rim. The infraorbital landmarks are represented as a surface rendering in gray. The experimental group (negative PC scores) is characterized by an infraorbital depression as demonstrated by the posterior and medial deformation of the spline. In contrast, the infraorbital region of the control/sham group (positive PC scores) is characterized as ‘inflated’. This is demonstrated by the anterior and lateral deformation in the spline along the infraorbital region. The depression in the experimental group is due to a reorientation of the zygomatic aspect of the infraorbital region relative to the maxillary region. Variation in the infraorbital region is further illustrated by the computed tomography renderings in B and C. The infraorbital region of the experimental group (B) is coronally oriented whereas the infraorbital region of the control/sham group (C) is parasagittally oriented. Visualizations of the mandible and cranial base, as line segments, were excluded from this figure to aid in the visualization of other morphological features. rh, rhinion; l, lambda; ba, basion; pr, prosthion.