Journal of
Anatomy
J. Anat. (2010) 216, pp48–61
doi: 10.1111/j.1469-7580.2009.01162.x
Sutural growth restriction and modern human facial evolution: an experimental study in a pig model Nathan E. Holton,1,2 Robert G. Franciscus,1,2 Mary Ann Nieves,3 Steven D. Marshall,1 Steven B. Reimer,4 Thomas E. Southard,1 John C. Keller5 and Scott D. Maddux2 1
Department of Orthodontics, University of Iowa, Iowa City, IA, USA Department of Anthropology, University of Iowa, Iowa City, IA, USA 3 Department of Veterinary Microbiology and Preventative Medicine, Iowa State University, Ames, IA, USA 4 Department of Veterinary Clinical Sciences, Iowa State University, Ames, IA, USA 5 The Graduate College, University of Iowa, Iowa City, IA, USA 2
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. Key words archaic Homo; canine fossa; facial retraction; facial size reduction; infraorbital shape; Sus scrofa; sutural rigid plate fixation.
Introduction A retracted facial skeleton and an overall reduction in facial size are among the defining characteristics of Homo sapiens (e.g. Weidenreich, 1941; Moss & Young, 1960; Franciscus, 1995; Vinyard & Smith, 2001; Ponce de Le´on & Zollikofer, 2001; Lieberman et al. 2002; Trinkaus, 2003).
Correspondence Nathan E. Holton, Department of Orthodontics, S219 Dental Science Building, University of Iowa, Iowa City, IA 52242, USA. T: +319 335 7288; E:
[email protected] Accepted for publication 22 September 2009 Article published online 19 November 2009
Various other characteristics of the facial skeleton that distinguish H. sapiens from archaic Homo are thought to be developmentally linked to facial skeleton reduction. For example, a reduction in modern human external nasal breadth dimensions has been causally linked to a decrease in absolute lower facial projection (Holton & Franciscus, 2008). Similarly, the unique morphology of the supraorbital (e.g. reduction in prominence) and infraorbital (e.g. presence of a canine fossa) regions has been tied to facial retraction and a reduction in overall facial size in modern humans (Weidenreich, 1941; Moss & Young, 1960; Lieberman, 2000; Ravosa et al. 2000; Vinyard & Smith, 2001; Maddux & Franciscus, 2009). A reduction in the size of the pharyngeal space (e.g. McCarthy & Lieberman, 2001;
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Lieberman et al. 2002) and the prominence of the mentum ossuem are also probably a function of variation in anteroposterior facial dimensions (Durand & Hunt, 2008; Scott et al. 2009; Marshall et al. in press). A clearer understanding of the ultimate evolutionary causes of facial reduction and retraction in H. sapiens, be they primarily neutral (e.g. Hublin, 1998; Franciscus, 2003; Roseman & Weaver, 2004; O’Connor et al. 2005; Holton & Franciscus, 2008) or adaptive (Trinkaus, 1986, 2000; Smith & Paquette, 1989; Franciscus & Trinkaus, 1995; Lieberman, 2008), is predicated on our ability to identify the specific craniofacial developmental dynamics that affect variation in facial size and projection. Evolutionary modifications of modern human craniofacial form result from heterochronic shifts in development and alterations of both pre-natal and post-natal growth allometries. The precise developmental dynamics that account for the evolutionary modifications in the overall size and increased retraction of the facial skeleton in modern humans are complex, multi-factorial processes that involve intrinsic genetic and epigenetic factors throughout growth and development (e.g. Atchley & Hall, 1991; Herring, 1993). For example, as a key structural interface between the neurocranium and viscerocranium, growth and development of the cranial base has been the focus of much research regarding craniofacial variation (Moss & Young, 1960; Enlow, 1990; Ross & Ravosa, 1993; Lieberman et al. 2000; McCarthy & Lieberman, 2001; Bastir & Rosas, 2006; Bastir et al. 2006; Lieberman et al. 2008). In particular, cranial base angulation has been the subject of numerous analyses regarding facial form and projection in primates. For example, due to the effects of ‘spatial packing’, an increase in brain volume, relative to the length of the cranial base, results in an increase in the flexion between the pre-chordal and post-chordal components (e.g. Ross & Ravosa, 1993; Ross & Henneberg, 1995; Spoor, 1997; Lieberman et al. 2008). Reduction in facial size and the effects of ‘facial packing’ additionally account for variation in cranial base angle (Lieberman et al. 2008). Similarly, the relative size and shape of the cranial fossae are associated with variation in facial projection with recent humans characterized by a relative increase in anterior cranial base length (Spoor et al. 1999; Lieberman, 2000; Lieberman et al. 2002). The size and shape of the middle cranial fossa are also associated with variation in facial projection and length in recent humans (Bastir & Rosas, 2006) as well as between modern humans and archaic Homo (Seidler et al. 1997; Lieberman et al. 2002; Bastir et al. 2008). Whereas growth of both the midline and lateral components of the cranial base ceases early in ontogeny (Lieberman & McCarthy, 1999; Lieberman, 2000; Bastir et al. 2006), the facial skeleton continues to grow into adulthood (e.g. Bastir et al. 2006; Edwards et al. 2007; Holton & Franciscus, 2008). Therefore, whereas the cranial base probably
places developmental constraints on the degree of morphological variation during growth of the facial skeleton proper, it is nonetheless informative to assess growth dynamics intrinsic to the facial skeleton that may also contribute to differences in facial size and projection. For example, variation in pre-maxillary suture patency in archaic and modern humans (Maureille & Bar, 1999) as well as population variation within extant humans (Mooney & Siegel, 1986) likely accounts for some of the variation in anteroposterior facial dimensions. Insight into the potential evolutionary significance of alterations in growth and development can be gained by examining congenital growth abnormalities in the craniofacial skeleton (e.g. Cox et al. 2006; Zollikofer & Ponce de Le´on, 2006). Particularly relevant to evolutionary modifications in modern human facial form is a condition known as vertical maxillary excess. This abnormality arises from vertical overgrowth of the maxilla relative to other facial bones and results in a condition often referred to as ‘long-face syndrome’ (Schendel et al. 1976; Schendel & Carlotti, 1985). Individuals with vertical maxillary excess are dolichofacial, developing a characteristic elongation of anterior vertical facial dimensions, a steep mandibular plane and frequently a Class II malocclusion and ⁄ or anterior open bite. If the condition goes untreated during childhood, patients typically require orthognathic surgery (Bell & McBride, 1977; Hoppenreijs et al. 1997). In a previous study, Southard et al. (2006) explored the feasibility of attenuating excessive maxillary growth via rigid plate fixation as a means of treating vertical maxillary excess. Rigid plates were affixed across the zygomaticomaxillary and frontonasomaxillary sutures in a pig model to restrict maxillary growth and, as a result, the experimentally plated pigs (after 2 months post-surgical growth) clearly exhibited a reduction in anterior–posterior facial dimensions relative to a control sample. Interestingly, and unexpectedly, the reduction in facial length in the experimental pigs was accompanied by a markedly depressed and reoriented infraorbital region. Although this study was exploratory, and the sample sizes were too small for statistical analysis, the induced size and shape alterations were intriguingly parallel to those that accompany the emergence of modern human facial form in the Later Pleistocene, and raise questions about the precise role of variation in intrinsic facial length, in addition to alterations in cranial base morphology, in the evolution of modern human facial form. Here we report the results of a more elaborate study, using a pig model, to more fully examine the effects of experimentally induced facial length reduction via restriction of circummaxillary sutural growth sites on differential size and shape alterations (e.g. infraorbital region) of the skull and to assess the potential role of intrinsic facial size reduction as one of a number of factors underlying the evolution of modern human facial form.
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Materials and methods Ten female Sus scrofa sibship cohorts, each consisting of three individuals, were allocated to one of three trial groups (i.e. experimental, sham and control). In the experimental group (n = 10), rigid microplates were bilaterally affixed across the zygomaxillary, frontonasal and nasomaxillary sutures at 2 months of age. Oxytetracycline (200 mg mL)1, Liquamycin LA200, Pfizer Pharmaceuticals) was administered (20 mg kg)1) as an antibiotic at 1 day prior to surgery and at 5 and 10 weeks post-surgery. As a pre-medication, the pigs were given a combination of medetomidine HCl (1 mg mL)1, Dormitor, Orion Pharma, Orion Corporation, Espoo, Finland), 0.08 mg kg)1 butorphanol tartrate (0.5 mg mL)1, Torbutrol, Fort Dodge Animal Health, Fort Dodge, IA, USA) and 0.2 mg kg)1 glycopyrrolate (0.2 mg mL)1, Robinul, Baxter Healthcare Corporation, Deerfield, IL, USA). Ketamine HCl (100.0 mg mL)1, Ketaset, Fort Dodge Animal Health) was used as the induction agent and was delivered intramuscularly at a dose of 10.0 mg kg)1. All pigs were intubated intratracheally and placed on 1.0% isoflurane (Forane, Baxter Healthcare Corporation) to maintain a surgical plane of anesthesia. All pigs were administered intravenous crystalloid fluids through an ear vein while anesthetized. To affix the rigid plates over the zygomaxillary sutures, an incision was made approximately 10.0 mm ventral and 20.0 mm caudal to the medial canthus of the eye parallel to and over the zygomatic arch to the level of the maxilla to center over the zygomaticomaxillary suture (Fig. 1). A periosteal elevator was used to expose the suture. A straight pediatric 1.5-mm commercially pure titanium microplate (KLS-Martin L. P., Jacksonville, FL, USA) was rigidly fixed using four 1.5-mm titanium alloy cross-driven microscrews on opposite sites of the plate (i.e. two on each side) and farthest from the suture line to bridge the sutures. For the frontonasal and nasomaxillary sutures, an incision centered over the frontonasal suture was made over the most lateral edge of the frontal bone extending 5.0 mm dorsal to the medial canthus of the eye and extending 40.0 mm cranially. The periosteum was elevated to expose the frontonasal and naso-
Frontonasomaxillary
Zygomaticomaxillary 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.
maxillary sutures. A 1.5-mm commercially pure titanium L-shaped pediatric microplate was contoured and rigidly fixed to bridge both the frontonasal and nasomaxillary sutures by placing two screws in each bone segment avoiding direct contact with the suture line (Fig. 1). All screw holes were drilled using a 1.0-mm drill bit and the screws placed manually without pre-tapping due to the softness of the bone. The sham group (n = 10) underwent an identical surgical procedure, also at 2 months of age, but received only microscrew implantation at the zygomaxillary, frontonasal and nasomaxillary sutures. Plates were temporarily placed across sutures as previously described for pigs in the experimental group to ensure equal spacing of the screws across the sutures. Once the holes were drilled, the plates were removed and the screws were implanted. The control group (n = 10) underwent no surgical procedure. To prevent trauma after surgery, the pigs were housed separately until the incisions had healed. All pigs were fed the same diet to eliminate the potential effects of variation in dietary consistency on facial growth (Watt & Williams, 1951; Moore, 1965; Beecher & Corruccini, 1981; Corruccini & Beecher, 1982; Beecher et al. 1983; Ito et al. 1988; Ciochon et al. 1997; Ulgen et al. 1997; Katsaros et al. 2002; Lieberman et al. 2004). Water was provided ad libitum. To determine whether the surgery differentially affected the dietary behavior of the pigs, and thus potentially their growth, pigs in all three trial groups were weighed at the age of 2 months and again at 6 months. Following 4 months post-surgical growth (i.e. at 6 months of age), all pigs were killed using a combination of 2.5 mL xylazine HCl (100 mg mL)1, Rompun, Bayer HealthCare, Shawnee Mission, KS, USA) and 2.5 mL Ketamine HCl (100 mg mL)1, Ketaset, Fort Dodge Animal Health) added to 5 mL of Tiletamine HCl ⁄ Zolaepam HCK (Telazol, 100 mg mL)1, Fort Dodge Animal Health). This was administered at 1 mL 100 pounds)1 intramuscularly as a tranquilizer and 30 mL of 26% sodium pentobarbital and 7.8% isopropyl alcohol was administered intravenously as the euthanasia solution. All experimental procedures were approved by The University of Iowa Institutional Animal Care and Use Committee. One control pig did not survive to age 6 months and the cranium of one sham pig was disarticulated during post mortem processing. These individuals were not included in our analysis, reducing both the sham and control sample sizes to n = 9 each. Differences in overall facial size and shape were examined using both linear measurements and geometric morphometric assessments of coordinate landmark data. Measurements (Table 1) were selected to reflect aspects of the overall facial, neurocranial and mandibular form with an emphasis on those that have featured prominently in discussions of facial reduction and retraction in the genus Homo. Anteroposterior dimensions of the facial skeleton were measured as nasal bone length (nrh), facial length (n-pr), palate length (pr-st) and mandibular length. The degree of facial projection relative to the anterior cranial base was measured as the distance between prosthion and a vertical line from the foramen cecum (pr-fc) perpendicular to the mandibular plane. In addition, nasopharyngeal length was measured as the distance between staphylion and basion (st-ba). Cranial base angle (CBA1) (e.g. Lieberman et al. 2000) was measured as the angle between the basion–sella line and the foramen cecum–sella line (Fig. 2). All measurements were taken from dry skulls with the exception of those involving cranial base morphology (i.e. fc-s-ba and pr-fc), which were taken
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Table 1 Cranial and mandibular measurements used in univariate analysis. Measurement
Description
Parietal length (b-l) Frontal length (b-n) Maximum cranial breadth (eu-eu) Bi-zygomatic breadth (zy-zy) Nasal length (n-rh) Facial length (n-pr) Palate length (pr-st) Facial retraction (pr-fc) Nasopharynx length (st-ba) Mandibular length Mandibular ramus breadth Cranial base angle (ba-s-fc)
Distance from bregma (b) to lambda (l) Distance from bregma (b) to nasion (n) Bi-eurion (eu) distance Bi-zygion (zy) distance Distance from nasion (n) to rhinion (rh) Distance from nasion (n) to prosthion (pr) Distance from prosthion (pr) to staphylion (st) Horizontal distance from prosthion (pr) to foramen cecum (fc) parallel to mandibular plane Distance from staphylion (st) to basion (ba) Maximum length of the mandible horizontal to the mandibular plane Minimum anteroposterior distance across the mandibular ramus Angle formed by basion (ba), sella (s) and foramen cecum (fc)
from computed tomography scans. Differences in measurement values among the experimental, sham and control groups were evaluated with non-parametric significance tests using NCSS (Hintze, 2001) and incorporated a modified false discovery rate adjustment for the number of multiple comparisons in our study (a = 0.016) following Narum (2006). To further evaluate size and shape differences in the cranium, a series of 3D coordinate landmarks (Fig. 3) were selected to represent detailed aspects of the facial skeleton, neurocranium (Fig. 3A) and mandible (Fig. 3B). To capture the complex topography of the infraorbital region, a scaled grid was projected onto the surface of the facial skeleton following Maddux & Franciscus (2009). The grid 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. From this larger grid, a smaller grid (Fig. 3C) with a subset of k = 24 landmarks was selected and ranged from the anterior maxilla to the body of the zygomatic. The majority of the landmarks were taken on dry skulls; however, the internal cranial base landmarks (i.e. foramen cecum and sella) were taken from computed tomography scans. The
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.
landmarks taken from these different sources were combined into a single set of landmarks using DVLR 4.12 (Raaum, 2006). Shape differences were quantitatively assessed using principal components analysis of Procrustes scaled shape variables and qualitatively assessed using thin-plate splines in MORPHOLOGIKA (O’Higgins & Jones, 1998). To assess the relationship between size and shape variables, individual principal component (PC) scores were regressed against centroid values derived from the coordinate landmarks.
Results No significant differences were found between the control and sham groups for any variables in the univariate analysis or the multivariate geometric morphometrics analysis; therefore, these pigs were combined into a single control ⁄ sham trial group. Body weights for the three trial groups taken at ages 2 and 6 months are shown in Table 2. There were no significant differences at either age (i.e. 2 and 6 months), indicating that the surgery did not affect the dietary habits of the experimental and sham pigs. Thus, any differences in facial size among the trial groups cannot be attributed to food intake. A visual comparison between a resulting representative control pig and an experimental pig is shown in Fig. 4 and the univariate statistical results are shown in Table 3. With respect to the neurocranium, frontal bone length (bregma-nasion) was statistically significantly reduced in the experimental group (9.1%) with a mean value of 79.7 mm compared with a mean value of 87.7 mm in the control ⁄ sham group (P < 0.001). In contrast, there were no significant differences in parietal bone length (b-l) (P = 0.870), maximum cranial breadth (eu-eu) (P = 0.538) or bi-zygomatic breadth (zy-zy) (P = 0.150). Similarly, there was no difference in cranial base angle (b-s-fc) (P = 0.274). The facial skeleton of the experimental group exhibited a reduction in anteroposterior dimensions compared with the control ⁄ sham group. Nasal bone length (n-rh) in the experimental group (mean 96.6 mm) was statistically significantly
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Table 2 Descriptive statistics and Kruskal–Wallis results for body weights (kg) of control, sham and experimental pigs at age 2 and 6 months.
A
Control
Sham
Experimental
Age
Mean (SD)
Mean (SD)
Mean (SD)
P
2 months 6 months
18.4 (4.6) 114.9 (13.6)
18.6 (4.3) 112.7 (15.1)
17.9 (4.3) 110.7 (16.2)
0.899 0.911
There were no significant differences among the groups at either age.
B
C
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.
reduced (P < 0.001) by 12.6% compared with the control ⁄ sham group (mean 110.5 mm). Similarly, overall facial length (n-pr) was statistically significantly shorter (P < 0.001) in the experimental group (10.1%) with a mean value of 114.1 mm compared with 126.9 mm for the control ⁄ sham group. The facial skeleton of the experimental group was also posteriorly positioned relative to the
neurocranium (i.e. retracted) as demonstrated, first, by a reduction (8.2%) in the horizontal distance from the prosthion to the foramen cecum (pr-fc) (P < 0.001) and, second, from the statistically significant reduction (P = 0.001) in the length of the nasopharynx (st-ba) (6.5%). In contrast to other facial length measurements, palate length (pr-st) was not reduced in the experimental group (P = 0.360). Mandibular growth was also affected by sutural fixation but not to the degree observed in the facial skeleton. There was a reduction in both mandibular length (3.9%) and mandibular ramus breadth (5.7%); however, only the difference in mandibular ramus breadth attained statistical significance (P = 0.010). Interestingly, even with the discrepancy between the reduction in sagittal craniofacial and mandibular growth, post-canine malocclusion occurred in only three of nine experimental pigs (excluding one cohort in which malocclusion occurred even in the control). The results of the geometric morphometrics analysis revealed clear differences in craniomandibular shape between the experimental and control ⁄ sham groups. PC1, which explained 32.3% of the variation in the sample, separated the experimental pigs from the controls and shams (Fig. 5). Individual PC scores along the first principal component were statistically significantly different (P < 0.001) and the distribution of individuals along this axis revealed minimal overlap between the experimental and control ⁄ sham trial groups. With respect to the midsagittal plane (Fig. 6), there were two major morphological differences between the experimental and control groups along PC1. First, the experimental group exhibited a relative reduction in anteroposterior snout dimensions. Although the dorsal snout was reduced in overall length, the palatal region maintained its length and was more posteriorly positioned, i.e. as the face of the experimental pigs became reduced in length, the palate became more retracted relative to the neurocranium. This had the effect of reducing the relative length of the nasopharyngeal space. Variation along PC1 was statistically significantly correlated with centroid size (r = 0.43; P = 0.023) with the experimental pigs exhibiting a statistically significantly smaller centroid size (P = 0.003) (Fig. 7) relative to the control ⁄ sham pigs.
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A
B
Fig. 4 Comparison of a representative control (A) and a representative experimental (B) pig.
Table 3 Descriptive statistics and Mann–Whitney U-test results for cranial and mandibular measurements. Control ⁄ sham
Experimental
Measurement (mm)
Mean (SD)
Mean (SD)
Parietal length (b-l) Frontal length (b-n) Maximum cranial breadth (eu-eu) Bi-zygomatic breadth (zy-zy) Nasal length (n-rh) Facial length (n-pr) Palate length (pr-st) Facial retraction (pr-fc) Nasopharynx length (st-ba) Mandibular length Mandibular ramus breadth Cranial base angle (ba-s-fc)
25.9 87.7 75.9 151.1 110.5 126.9 158.4 144.0 80.4 204.8 65.1 175.3
27.6 79.7 76.3 149.5 96.6 114.1 158.2 132.1 75.2 196.9 61.4 176.3
(3.9) (3.5) (3.2) (3.3) (7.1) (7.0) (7.8) (8.5) (3.5) (9.4) (3.5) (3.0)
(4.4) (3.6) (4.4) (4.0) (5.9) (5.0) (9.4) (5.2) (3.0) (10.0) (3.7) (2.8)
Percentage difference 6.6 )9.1 0.5 )1.1 )12.6 )10.1 )0.1 )8.2 )6.5 )3.9 )5.7 )0.6
P* 0.870 < 0.001 0.538 0.150 < 0.001 < 0.001 0.360 < 0.001 0.001 0.029 0.010 0.274
Significant differences are in bold. *Statistical significance determined using a modified false discovery rate adjustment for multiple comparisons (a = 0.016) following Narum (2006). b, bregma; l, lambda; n, nasion; eu, eurion; zy, zygion; rh, rhinion; pr, prosthion; st, staphylion; fc, foramen cecum; ba, basion; s, sella.
In addition to shape differences in the facial skeleton along PC1, there was a reorientation of the snout relative to the neurocranium. In the experimental pigs, the snout was more dorsally oriented, resulting in a more acute angle formed between the nasal and frontal bones. This was due, at least in part, to a relative shortening of the frontal bone in the experimental pigs as noted above. The mandibular corpus followed the reorientation of the snout as the mandibular ramus was more vertically oriented relative to the corpus (i.e. a more acute gonial angle) in the experimental pigs. Although the snout was reoriented relative to the neurocranium, this reorientation was independent of variation in cranial base angle. Figure 8 shows variation in the midsagittal plane with the cranial base angle (fc-s-ba) added to the visualization and the mandible removed (note that the same landmarks were used in both splines and it is only the line segments used to visualize the mandible that have been removed). Although the orientation of the cranial base as a whole varied with the orientation of the neurocranium relative to the facial skeleton, there
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.
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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. 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).
was no difference in the degree of cranial base flexion between the experimental and control ⁄ sham groups. Thus, the reorientation of the facial skeleton relative to the neurocranium resulting from the experimental modification was independent of variation in the cranial base. In addition to changes in relative facial lengths and orientation, there was considerable shape modification to the infraorbital region. Figure 9 is a thin-plate spline oriented transversely through the infraorbital region. The surface rendering used to assess shape in the infraorbital region is not pictured so as not to obstruct the view of the thin-plate spline deformation. The infraorbital region of the experimental pigs was characterized by a deep depression near the articulation of the maxilla and zygomatic (see also Fig. 4). This was evident from the posterior and medial deformation of the spline in the infraorbital region. In contrast, the control ⁄ sham pigs showed a more ‘inflated’
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. ª 2009 The Authors Journal compilation ª 2009 Anatomical Society of Great Britain and Ireland
Sutural growth restriction and modern human facial evolution, N. E. Holton et al. 55
A
B
C
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.
infraorbital region, relative to the experimental pigs, as there was an anterior and lateral deformation of the spline in the infraorbital region. There was one further important shape difference in the infraorbital region when viewed laterally. Figure 10 is a sagittally oriented thin-plate spline lateral to the midline approximately through the frontolacrimal suture along the orbital rim. In the control ⁄ sham group, the infraorbital plane faced superiorly, whereas the infraorbital plane in the experimental group was oriented inferiorly.
Discussion The results of this study indicate that facial growth restriction via rigid plate fixation of the circummaxillary sutures in a pig model produces highly predictable and significant
alterations of facial form that parallel the morphological differences observed between modern and archaic Homo. Relative to the controls, the experimental sample exhibited a significant reduction in the anteroposterior dimensions of the facial skeleton. This included a reduction in overall length (e.g. na-pr length) and a reduction in the superior rostrum (e.g. nasal bone length), and was accompanied by a general reduction in overall facial size as documented by smaller centroid size values. In addition, due to the plating of the frontonasomaxillary suture, there was a significant reduction in frontal bone length and a general reorientation of the facial skeleton relative to the neurocranium. Other linear dimensions of the neurocranium (i.e. length and breadth dimensions) were unaffected by the plating. The experimental sample was further characterized by a more retracted facial skeleton as demonstrated by the
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56 Sutural growth restriction and modern human facial evolution, N. E. Holton et al.
A
B
C
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.
reduction in the distance between the snout and the anterior cranial base. This was also evident from the geometric morphometric analysis, which revealed the snout to be posteriorly displaced. The marked facial retraction was further associated with a reduction in the length of the nasopharynx, which resulted from a combination of facial length reduction coupled with the maintenance of palatal length in the experimental sample. Thus, as growth was restricted in the more superior aspects of the rostrum (i.e. superior to the dentognathic region), the palate was shifted posteriorly toward the basioccipital. Interestingly, although facial projection varies with cranial base morphology in hominids and in an experimental mouse model (Spoor et al. 1999; Lieberman et al. 2000, 2000, 2008), our results revealed no significant differences in the cranial base form. Facial reduction, in our pig model, was further associated with a significant alteration in the shape of the infraorbital region. As a result of zygomaxillary sutural fixation, the experimental sample developed an infraorbital depression. This feature was manifest as a deep concavity that resulted from a reorientation of the zygomaxillary region from the parasagittal, evident in the control ⁄ sham pigs, to the coronal plane. In addition, the infraorbital plane was oriented inferiorly in contrast to the superior orientation that characterized the control ⁄ sham group. Parallel contrasts in infraorbital shape and orientation between archaic Homo and
H. sapiens have been seen as important characteristics in both functional (Smith, 1983; Rak, 1986; Demes, 1987) and phylogenetic (Stringer et al. 1984; Bermu´dez de Castro et al. 1997; Arsuaga et al. 1999; Lieberman et al. 2002; Trinkaus, 2006) interpretations of modern human craniofacial evolution. The presence of an infraorbital depression and the inferior orientation of the infraorbital plane, in our experimental sample, are associated with a reduction in the overall size, a relationship that has been documented in Middle and Late Pleistocene hominids (Maddux & Franciscus, 2009). In addition to the upper and midfacial skeleton, the mandible exhibited predictable changes in morphology. Specifically, the experimental group was characterized by a reduction in mandibular length and mandibular ramus breadth; however, only the latter attained statistical significance. Similarly, the experimental pigs were characterized by a reorientation of the mandibular corpus relative to the mandibular ramus as demonstrated by the thin-plate splines. The reorientation of the ramus probably explains the reduction in mandibular length as the superior aspect of the posterior border of the ramus was positioned more anteriorly in the experimental group. These alterations in mandibular morphology, as a secondary consequence of facial reduction, are broadly similar to studies in humans that have established morphological integration between
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mandibular plane angle and midfacial growth (Sassouni, 1969; Bhat & Enlow, 1985; Bastir & Rosas, 2004). Similarly, mandibular ramus morphology is developmentally integrated with the midline cranial base and middle cranial fossa (Enlow et al. 1982; Enlow & Hans, 1986; Bastir et al. 2003; Bastir & Rosas, 2005). Both mandibular ramus breadth and the orientation of the ramus have been shown to vary with alterations in the orientation of these neurocranial structures. Thus, the relative reorientation of the facial skeleton and neurocranium in our experimental group would seem to have predictably altered mandibular morphology in a manner consistent with previous studies. Whereas in the present study facial sutures were surgically modified to restrict facial growth, variation in sutural growth, due to differences in the timing of suture fusion ⁄ patency, has been suggested as a contributing factor to differences in anteroposterior facial dimensions in modern and archaic Homo. In extant human subadults, the premaxillary suture fuses earlier than Neandertal subadults (who presumably exhibited the pleisiomorphic condition of prolonged premaxillary suture patency), thus reducing the potential for additional anteroposterior growth (Maureille & Bar, 1999). A similar pattern in premaxillary sutural patency variation has also been documented in extant human populations exhibiting variation in lower facial prognathism (Mooney & Siegel, 1986). The key observation in both cases is that earlier sutural fusion is clearly associated with reduced lower facial projection in adults. It is also interesting to note that premature synostosis of the premaxillary suture in animal models can affect other aspects of facial form such as anterior cranial base morphology (Mooney et al. 1992; Ruan et al. 2008). The precise dynamics that govern facial sutures in terms of growth and patency are not well understood. Whereas the regulation of neurocranial suture patency is known to come from the dura mater, the role of tissue interaction in facial suture morphogenesis and regulation is less clear (Opperman, 2002). However, the expression of transforming growth factor-b isoforms in the frontonasal and transpalatal sutures appears to be regulated by the surrounding nasal capsular cartilages, suggesting that these may play a significant role in maintaining facial suture patency (Adab et al. 2002, 2003). Nevertheless, in contrast to the premaxillary suture, other facial sutures (e.g. the zygomaxillary suture) in humans do not typically fuse until as late as the seventh decade (see Kokich, 1986) indicating that, unlike the premaxillary suture, there is no straightforward relationship between sutural patency ⁄ fusion and the promotion ⁄ cessation of growth. Thus, although cessation of premaxillary sutural growth is tied to sutural fusion, this is not the case for others such as the zygomaticomaxillary suture. However, it is worth noting that we have observed complete fusion of facial sutures in crania that are considerably younger than the seventh decade in recent humans and fossil hominids. For example, the Levantine Qafzeh 6
early modern human (dated to ca. 100 kya), probably 20–40 years of age at death, shows bilateral nasomaxillary suture fusion to the extent that the original suture course and location cannot be determined (Vandermeersch, 1981; R.G.F., personal observation). Differential sutural growth and premature synostosis as exhibited in Apert and Crouzon syndromes, however, can result in hypoplasia of the maxillary complex and thus a retrusive midface (e.g. Cohen & Kreiborg, 1996; Krieborg, 2000; Rice, 2008). Both syndromes are characterized, in part, by synostosis of the calvarial sutures and cranial base synchondroses. In addition, the maxilla exhibits a reduction in sutural growth and in some cases the sutures of the maxillary complex (e.g. palatal sutures) are prematurely fused (Kreiborg, 2000). However, it is not entirely clear whether reduced maxillary sutural growth results from a change in the growth potential of the sutures themselves or from developmental alterations of growth centers that drive the growth of the maxillary complex (see Adab et al. 2003). Sutural growth is promoted by developmentally induced biomechanical strains such as intracranial pressure on neurocranial sutures (e.g. Cohen, 1993) and nasal septal traction on facial sutures (Wexler & Sarnat, 1961; Latham et al. 1975; Mooney et al. 1989; Roberts & Lucas, 1994; Wealthall & Herring, 2006). Although the present study was designed to reduce anterior growth of the facial skeleton by minimizing the influence of developmentally induced strains on facial suture growth, the reduction in growth may also be functionally driven. It is well documented that both neurocranial and facial sutures function to dissipate the high-magnitude strains produced during mastication. Dynamic masticatory strains can, for example, exceed 1000 microstrain in the zygomatico–squamosal and premaxillary sutures in pigs (e.g. Herring & Mucci, 1991; Rafferty et al. 2003). These functionally induced strains promote increased fibroblastic and osteoblastic activity, and thus influence facial growth (e.g. Herring & Mucci, 1991; Rafferty & Herring, 1999; Herring & Teng, 2000; Bresin & Kiliaridis, 2002; Kopher & Mao, 2002; Mao et al. 2003; Rafferty et al. 2003; Lieberman et al. 2004; Katsaros et al. 2006; Mao, 2006). The use of rigid fixation in the experimental group, however, may reduce or alter the ability of plated sutures to adequately dissipate masticatory strain (e.g. Freeman et al. 1997), thus affecting growth. The lack of a significant difference in body weight (and thus food consumption) among the trial groups suggests that the experimental group was subjected to the same level of masticatory strain as the control ⁄ sham group. However, the magnitude of strain at the sutures may have been minimized, thus affecting the distribution and orientation of these strains in the experimental group. This altered strain environment may account for the reorientation of the facial skeleton relative to the neurocranium in the experimental group as reduced masticatory strain in rats
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58 Sutural growth restriction and modern human facial evolution, N. E. Holton et al.
produces the same reorientation of the facial skeleton (Kiliaridis et al. 1985; Bresin & Kiliaridis, 2002). The retraction of the facial skeleton may have further affected masticatory function by positioning the dental arcade closer to the masticatory musculature and temporomandibular joint, thus altering the mechanics of masticatory force production. For example, a more posteriorly positioned bite point, in humans, is associated with reduced electromyographic activity in the masseter and anterior temporalis (Spencer, 1998). Given the more posterior position of the dentition in the experimental pigs, masticatory muscle activity may have been similarly affected. This dynamic may help to explain the reduction in mandibular ramus breadth in our experimental pigs as the size and shape of the mandibular ramus is influenced by masticatory muscle size, force production and orientation (Pratt, 1943; Washburn, 1947; Horowitz & Shapiro, 1951; Avis, 1959, 1961; Moore, 1967; Schumacher et al. 1979; Byrd et al. 1990; Carter & Harkness, 1995; Navarro et al. 1995; Yonemitsu et al. 2007; Holton, 2009). It should be noted, however, that no changes were noted in the gonial region, which serves as the insertion for the masseter and medial pterygoid. The evolutionary and ontogenetic development of the modern human facial skeleton was a complex, multifactorial process. The present study was designed to examine only one specific aspect of facial form, namely, variation in anteroposterior facial dimensions as a function of sutural growth restriction. By plating the circummaxillary sutures, we have modeled facial size reduction and concomitant shape changes in the infraorbital region that parallel morphological alterations between archaic and recent humans. Nevertheless, it is important to emphasize that the underlying dynamics that account for variation in the size and shape of the facial skeleton are numerous and complex with many aspects of morphology that differentiate modern and archaic Homo determined early in ontogeny (e.g. Williams, 2000, 2006; Ponce de Le´on & Zollikofer, 2001, 2006). For example, mesenchymal condensation size and shape determination is a significant prenatal developmental factor that influences variation in craniofacial form (Atchley & Hall, 1991; Hall & Miyake, 1995, 2000). Furthermore, growth hormone, as the primary regulator of postnatal growth (Pirinen, 1995), affects the size of the maxillary and mandibular complex (Pirinen et al. 1994; Kjellberg et al. 2000) as well as cranial base morphology (Spiegel et al. 1971; Scharf & Laron, 1972; Pirinen et al. 1994; Kjellberg et al. 2000). These factors, among others, surely played a significant role in the evolution of modern human craniofacial morphology including variation in facial length and retraction. It is also important to underscore that comparisons between our results and the morphological differences between archaic and modern humans may be further confounded by the general differences in facial growth between pigs and humans. Although pigs serve as a good
model for humans due to similarities in craniofacial size, dentition, diet and vertical stroke orientation (Ciochon et al. 1997; Herring et al. 2008), pigs exhibit an overall different facial growth trajectory than H. sapiens. Suids are characterized by a long rostrum that grows primarily in an anteroposterior direction, whereas H. sapiens is characterized by a considerably greater vertical growth vector. The ability to more clearly elucidate the underlying biological mechanisms that govern craniofacial morphology is necessary if we are to develop a more complete understanding of the evolution of the modern human facial skeleton. Particularly important in this regard is a better explanation of the developmental relationships among highly intercorrelated traits in order to make distinctions between proximate features and ultimate causal mechanisms. Such information is crucial in assessing the utility of morphological features that have been traditionally used to reconstruct phylogentic relationships within the genus Homo as well as in the determination of trait polarities (Trinkaus, 2006; Maddux & Franciscus, 2009). The present analysis takes a unique experimental approach in this regard and our results 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.
Acknowledgements We thank Dr. Dean Riedesel and Matt Keller for their assistance with the surgical procedures. We also thank Dan Lieberman, Erik Trinkaus and our reviewers for helpful discussion and comments regarding this manuscript. Additionally, we would like to acknowledge Ken Krizan for post-surgical specimen preparation. This research was funded by a University of Iowa OVPR BSFP Developmental Biology Grant.
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ª 2009 The Authors Journal compilation ª 2009 Anatomical Society of Great Britain and Ireland
