Developmental and Evolutionary Significance of the Zygomatic Bone

Abstract

The zygomatic bone is derived evolutionarily from the orbital series. In most modern mammals the zygomatic bone forms a large part of the face and usually serves as a bridge that connects the facial skeleton to the neurocranium. Our aim is to provide information on the contribution of the zygomatic bone to variation in midfacial protrusion using three samples; humans, domesticated dogs, and monkeys. In each case, variation in midface protrusion is a heritable trait produced by one of three classes of transmission: localized dysmorphology associated with single gene dysfunction, selective breeding, or long-term evolution from a common ancestor. We hypothesize that the shape of the zygomatic bone reflects its role in stabilizing the connection between facial skeleton and neurocranium and consequently, changes in facial protrusion are more strongly reflected by the maxilla and premaxilla. Our geometric morphometric analyses support our hypothesis suggesting that the shape of the zygomatic bone has less to do with facial protrusion. By morphometrically dissecting the zygomatic bone we have determined a degree of modularity among parts of the midfacial skeleton suggesting that these components have the ability to vary independently and thus can evolve differentially. From these purely morphometric data, we propose that the neural crest cells that are fated to contribute to the zygomatic bone experience developmental cues that distinguish them from the maxilla and premaxilla. The spatiotemporal and molecular identity of the cues that impart zygoma progenitors with their identity remains an open question that will require alternative data sets. Anat Rec, 299:1616-1630, 2016. © 2016 The Authors The Anatomical Record Published by Wiley Periodicals, Inc.

Keywords: FGFR-related craniosynostosis syndromes; New World monkeys; Old World monkeys; domesticated dogs; midfacial hypoplasia; midfacial retrusion; prognathism.

© 2016 The Authors The Anatomical Record Published by Wiley Periodicals, Inc.

Figures

Figure 1

Evolution of circumorbital bones of the dermatocranium from William King Gregory's, “Our face from fish to man” (1929) showing the change in zygomatic morphology over evolutionary time. The orbital series is figured in light gray while the zygoma or jugal is highlighted in yellow. I, Lobe‐finned fish, Devonian age; II, Primitive amphibian, Lower Carboniferous; III, Primitive cotylosaurian reptile, Permo‐Carboniferous; IV, Primitive theromorph reptile, Permo‐Carboniferous; V, Gorgonopsian reptile, Permian; VI, Primitive cynodont reptile, Triassic; VII, Primitive marsupial, Upper Cretaceous; VIII, Primitive primate, Eocene; IX, Anthropoid (female chimpanzee), Recent; Man, Recent. Gregory was an expert primatologist, paleontologist, and functional and comparative morphologist and a leading contributor to several theories of evolution including the “Palimpsest theory” (Gregory, 1947) and “Williston's Law” (Gregory, 1935). Adapted from Gregory's (1929) Figure 51, p.81.

Figure 2

Mouse (Mus musculus) skeletal development at three distinct developmental stages: A, Embryonic day 12.5 (E12.5); B, E15; C, postnatal day 0 (P0). Alizarin red (bone) and alcian blue (cartilage) staining was used at these three developmental stages.

Figure 3

Lateral view of canine skulls illustrates the shape and size variation of the zygoma (pseudo‐colored blue): A, boxer; B, Rottweiler; C, greyhound.

Figure 4

Skull reconstructions with measured landmarks (lateral, anterior, inferior views): A, human infant; B, labrador retriever; C, Macaca fascicularis. For more details on landmarks and semilandmarks measured on human infants see Heuzé et al. (2014). Landmarks measured on dogs include: nasion, nasale, anteriormost point on nasal bone, infradentale, premaxilla‐maxilla suture posterior to I2, first molar anteriormost point on alveolar bone, posterior nasal spine, premaxilla‐maxilla suture on hard palate, posteriormost point on zygomatic (temporal‐zygoma suture), superiormost point on zygomatic, inferiormost point on zygomatic (maxilla‐zygoma suture), zygoma‐lacrimal suture. Landmarks measured on monkeys include: nasion, nasale, infra dentale, premaxilla‐maxilla suture posterior to I2, anteriormost point on frontal‐zygoma suture, superiormost point on maxilla‐zygoma suture, inferiormost point on maxilla‐zygoma suture, maxillary tuberosity, pterygoid fossa, posterior nasal spine.

Figure 5

Morphological variation of the facial skeleton in infants diagnosed with FGFR‐related craniosynostosis syndromes and unaffected individuals. A, PCA of Procrustes shape coordinates of all landmarks and semilandmarks measured on the facial skeleton (left) and shape changes of the facial skeleton associated with the negative and positive extremes of PC1 (right); B, PCA of Procrustes shape coordinates of all landmarks and semilandmarks measured on the maxilla and premaxilla; C, PCA of Procrustes shape coordinates of all landmarks and semilandmarks measured on the zygoma.

Figure 6

Morphological variation of the facial skeleton in modern breed dogs. A, PCA of all landmarks measured on the left facial skeleton (left) and shape changes of the facial skeleton associated with the negative and positive extremes of PC1 (right); B, PCA of all landmarks measured on the left maxilla and premaxilla; C, PCA of all landmarks measured on the left zygoma.

Figure 7

Size variation among modern breed dogs based on natural log centroid size (lnCS) for the facial skeleton, maxilla, premaxilla, and zygoma (mean; whisker, ±0.95 confidence interval).

Figure 8

Morphological variation of the facial skeleton in Old World and New World monkeys. A, PCA of all landmarks measured on the left facial skeleton (left) and shape changes of the facial skeleton associated with the negative and positive extremes of PC1 (right).; B, PCA of all landmarks measured on the left maxilla and premaxilla; C, PCA of all landmarks measured on the left zygoma.