The placement of the Maxillo-Zygomatic suture in the primate midfacial

skeleton: An investigation on Old World Monkeys and New World Monkeys Qian Wang 1, Jana Makedonska 2, Craig Byron 3, David Strait 2

1Division of Basic Medical Sciences, Mercer University School of Medicine, 2Department of Anthropology, University at Albany , 3 Department of Biology, Mercer University

BackgroundCraniofacial sutures are major sites of bone expansion during postnatal skull growth

(Opperman, 2000). It is generally thought that the growth and morphology of craniofacial

sutures reflect their functional environment (Rafferty and Herring, 1999). Craniofacial

sutures can be viewed weak bone “growth” sites characterized by very different material

properties than the surrounding rigid skull bones; thence they must be shielded from

unduly high stresses so as not to disrupt vital growth processes and skeletal functions.

Thus, it is hypothesized that the placement of craniofacial sutures should maximize their

growth potentials yet minimize their negative biomechanical impacts, especially in areas

under high stress during dietary activities, such as the midface. Specifically, for any given

suture, it is hypothesized that suture position would be different in skulls of different form

and/or adapted to different dietary ecology.

In this pilot study, we investigated the position of the Maxillo-Zygomatic suture (MZS) and

the covariance patterns between zygomatic bone 3D sutural and geometric landmarks in a

sample including Old World Monkeys (OWMs) and New World Monkeys (NWMs) with the aim

to identify phylogenetic (including allometric) effects and distinctions among dietary

groups. Further, we studied the association of the zygomatic bone with maxillary and

premaxillary traits and neurocranial traits.

Results: Hypotheses # 1 is supported. Hypothesis # 2 not fully supposed by PC 2. Yet, zygomaxillare inferior is slightly more

laterally located in the robust NWM.

The comparison of species’ mean

configurations will certainly be more

suitable for assessing potentially

diet-driven variation in the position

of the zygomaxillare landmarks.

Acknowledgements

This research was supported by NSF-HOMINID grant BCS 0725126, BCS 0725183 and by Doctoral Dissertation Improvement Grant BCS 1028815.

References

Klingenberg C. 2011. MorphoJ: an integrated software package for geometric morphometrics. Molec Ecol Res 11: 353 – 357.

Makedonska J, Wright BW, Strait DS. 2012. The Effect of Dietary Adaption on Cranial Morphological Integration in Capuchins (Order Primates, Genus Cebus). The Effect of Dietary Adaption on Cranial Morphological

Integration in Capuchins (Order Primates, Genus Cebus). PLoS ONE 7(10): e40398. doi:10.1371/journal.pone.0040398

O’Higgins P, Jones N. 2006. Tools for statistical shape analysis. Hull York Medical School. http://sites.google.com/site/hymsfme/resources.

Opperman LA. 2000. Cranial sutures as intramembranous bone growth sites. Dev Dyn 219: 472 – 485.

Rafferty KL, Herring SW. 1999. Craniofacial sutures: morphology, growth and in vivoa masticatory strains. J Morphol 242: 167 – 179.

Wiley DF, Amenta N, Alcantara DA, Ghosh D, Kil YJ, Delson E,, Harcourt-Smith W, Rohlf FJ, St. John K, Hamann B. 2005. Evolutionary morphing. Proc IEEE Visualiz..

Summary and DiscussionHere we report a correlated shape change between the facial and temporal segments of the zygomatic bone, which

characterizes the distinction between OWMs and NWMs. In particular, OWMs have more medially placed zygomaxillare

superiors and more medially and anteriorly placed zygomaxillare inferiors. Although visual observations suggest that hard-

object feeding, robust NWMs might have more laterally placed zygomaxillare inferiors than the non-durophagous, gracile

NWMs, further analyses, and specifically the comparison of species’ means are needed. Finally, the zygomatic portion, located

in a highly strained area that supports the masseter muscle and involved in feeding function, is consistently more strongly

correlated with the rostral and molar units than with the zygomatic portion containing landmarks located on structures

supporting the brain and the eye. Thus, the placement of facial sutures and the covariance patterns involving the zygomatic

bone warrant careful ontogenetic, phylogenetic and biomechanical studies.

Materials and Methods33 3D landmarks were digitized using Landmark Editor (Wiley et al., 2005) on NextEngine surface

models of 158 crania (for details on methodology see Makedonska et al., 2012) of adult

anthropoid specimens housed at the Caribbean Primate Research Center, the Field Museum, the

American Museum of Natural History and the National Museum of Natural History.

Sample used in this study:

Landmarks used in this study, digitized on a

virtual C. apella s.s. cranial model.

Hypotheses # 1 and # 2 tested through Principal Components Analysis (PCA) carried out on the

Procrustes superimposed 3D coordinates of 22 zygomatic landmarks, not regressed on centroid

size and not pooled within species, parvorder or sex.

Hypothesis # 3 tested through within-configuration two-block Partial-Least Squares (PLS)

analyses evaluating the between-block multivariate correlation magnitude (RV coefficient) in two

competing partition scenarios:

PLS 1: developmental scenario: block 1 – a zygomatic unit including all zygomatic landmarks,

block 2 – a non-zygomatic unit including all rostral, molar and other neurocranial landmarks.

PLS 2: functional scenario: block 1 – a feeding unit including anterior zygomatic (zygomaxillare

inferiors, zygomatic roots, zygotemporales), rostral and molar landmarks, and block 2 – a

sensory unit including the zygomaxillare superiors, the fronto-malares, the pterions, the second

sutural landmark on the sphenoid, the external auditory meatus and the asterions.

Both scenarios were evaluated within species, on residuals from pooled-within-sex regression

on centroid size, in a selected subsample of species (those with larger sample sizes).

Morphometric analyses (PCA, PLS, regressions) carried out in MorphoJ (Klingenberg, 2011) and

Morphologika (O’Higgins and Jones, 2006).

HypothesesHypothesis # 1 :

Based on prior observations, we hypothesize that catarrhine crania are significantly distinct

from platyrrhine crania in that they concomitantly exhibit:

a. a more medially located zygomaxillare superior and a more anteriorly located

zygomaxillare inferior, resulting in a larger anterior zygomatic portion in the maxillary

plane, and

b. a more anteriorly located pterion indicating the degree of the posterior expansion of the

zygoma, which results in a smaller zygomatic contribution to the cranial vault.

This hypothesis concerns the development of the facial and the temporal parts of the zygoma,

and implies the presence of a correlated shape change between the anterior portion and

the posterior portion of the zygomatic.

Hypothesis # 2:

Hard-object-feeding, robust taxa (i.e., in this study, the tufted capuchin Cebus (Sapajus) apella

sensu stricto (s.s.) and the bearded saki Chiropotes satanas), are characterized by more

laterally located maxillo-zygomatic sutures than non-durophagous, gracile closely-related

taxa (i.e., in this study, the capuchin Cebus albifrons), since a laterally located MZS lies out

of the areas of highest feeding-related strain.

Hypothesis # 3:

The zygomatic landmarks, being linked through development, form a module or a suite of

autonomous and highly inter-correlated traits whose variation is relatively independent

from other non-zygomatic traits. The alternative hypothesis predicts that the functional

partition of the cranium estabishes correlations between skeletal traits that overrides their

developmental history; thus, it is expected that the anterior zygomatic will share stronger

correlations with the maxillary and premaxillary bones than with the posterior zygomatic.

Hypothesis # 3: In all examined species, the integration between the zygomatic “module” (that is all zygomatic landmarks

lumped in a single block) and the block containing the rest of the landmarks (molar, rostral, cranial vault), is higher than the

correlation between the feeding unit (part of zygomatic landmarks, rostral landmarks and molar landmarks) and the sensory

unit (part of zygomatic landmarks and posterior cranial vault landmarks). Some of the latter correlations are not significant

at the 0.05 level (see table below). Hence, the null Hypothesis # 3 is falsified.

Species Sample size

Cebus albifrons 18 (9♀, 9♂)

Cebus apella s.s. 21 (10♀, 11♂)

Chiropotes satanas 19 (9♀, 10♂)

Colobus guereza 17 (10♀, 7♂)

Colobus angolensis 13 (8♀, 5♂)

Cercopithecus

aethiops

17 (11♀, 6♂)

Erythrocebus patas 13 (7♀, 6♂)

Papio anubis 18 (4♀, 14♂)

Macaca mulatta 12 (6♀, 6♂)

Macaca nemestrina 3 (3♀)

Macaca arctoides 7 (6♀, 1♂)

Total 158 (83♀, 75♂)

Vectors at landmarks summarizing

the shape transformation from

NWM to OWM along PC 1

Vectors at landmarks summarizing the

shape transformation from colobines,

grivets and patas monkeys to

baboons along PC 2 (or from non-

durophagous to durophagous NWMs)

Non-pooled regressions of PC scores

on centroid size

Maxillo-zygomatic suture

Anterior zygomatic

Posterior zygomatic

Antero-posterior zygomatic boundary

Centroid size

predicts 66.18%

of the variation

along PC1

(p<0.0001)

Centroid size

predicts 16.41 % of

the variation along

PC1 (p<0.0001)

Species Correlation between the zygomatic

landmarks and the rest of landmarks

Correlation between the feeding

unit and the sensory unit

Cebus albifrons 0.526 (p=0.018) 0.445 (p=0.096)

Cebus apella s.s. 0.60 (p<0.001) 0.476 (p=0.01)

Chiropotes satanas 0.6435 (p<0.001) 0.597 (p<0.001)

Cercopithecus aethiops 0.5748 (p=0.002) 0.4865 (p=0.066)

Erythrocebus patas 0.622 (p=0.01) 0.4824 (p=0.179)

Colobus guereza 0.675 (p<0.001) 0.4642 (p=0.016)

Colobus angolensis 0.6646 (p<0.004) 0.582 (p=0.021)

Papio anubis 0.5794 (p=0.003) 0.561 (p=0.001)