Research on cranial suture biology has suggested there is biological information to be garnered from pattern of suture synostosis, the pattern being heritable (Falk et al., 1989; Wang et al., 2006a, b; Cray et al., 2008). Research also suggests a multifactorial explanation for cranial vault phenotype including heritability, diet, and biomechanics (Riesenfeld, 1967a; Aldridge et al., 2005a, b; Mooney and Richtmeier, in press). Cranial shape exhibits great genic and heritability dependent difference (Enlow and Hans, 1996; Hanihara, 1996; Gonzalez-Jose et al., 2005, 2008; Franklin et al., 2007). However, if populations are under similar environmental influences, there is an increased likelihood of intra-population similarities in craniofacial variation. These environmental influences can include diet and dietary transition (Gonzalez-Jose et al., 2005; Stynder et al., 2007), temperature (Riesenfeld, 1973; Roseman, 2004; Roseman and Weaver, 2004; Harvati and Weaver, 2006), and muscular development and loadings (Riesenfeld, 1967a; Kean and Houghton, 1982; Byron et al., 2004, 2006, 2008; Vecchione et al., 2007, 2010).
In Homo sapiens, early brain growth is a driving factor in determining the size and shape of the cranium (Weidenreich, 1941; Moss and Young, 1960; Moss, 1969; Moss and Salentijn, 1969; Enlow and Hans, 1996; Mooney et al., 2002; Richtsmeier et al., 2006). In early ontogeny, the expanding brain encapsulated by the dura mater creates a system of forces, placing pressure against the dura and skull tissues surrounding the brain, causing calvarial growth (Moss and Young, 1960; Moss, 1969; Moss and Salentijn, 1969; Enlow and Hans, 1996). Severe aberrations to early neural expansion can change normal growth trajectories, for example, hydrocephalus, anencephaly, and macrocephaly (Aldridge et al., 2005a, b). In addition, distinct cranial phenotypes can result from craniosynostosis, premature suture fusion that occurs prior to the completion of brain growth. For example, scaphocephaly, or pathological dolicocephaly (i.e., an excessively long, narrow cranium), results from premature sagittal suture fusion whereas pathological brachycephaly (i.e., an excessively short, wide cranium) results from premature coronal suture fusion (Babler and Persing, 1982; Enlow and Hans, 1996; Cohen and MacLean, 2000; Cohen, 2005). It is unclear whether these same patterns and relationships are observed for the normal ontogenetic development of the skull and eventual fusion. Because the cessation of neurocranial expansion and growth temporally precedes cranial suture remodeling and fusion (Meindl and Lovejoy, 1985; Cohen and MacLean, 2000), a causal mechanism affecting cranial shape is not expected. However, distinct cranial shapes may have different patterns of fusion reflecting their final phenotype. This study was designed to test the hypothesis that ectocranial suture synostosis pattern will differ according to cranial vault shape using Aleut skeletal material with varying cranial vault morphologies.
The Aleutian Islands are a chain of more than 300 small volcanic islands forming an island arc in the Northern Pacific Ocean. Contact with the Aleutian natives was made by sailors from Russia and the United States in the late 18th and 19th centuries, respectively. Ales Hrdlicka from the Smithsonian took several expedition in between 1910 and 1919 and abstracted historical demographic data on these people. The Aleutian Tradition began around 4450 BP and ended in 150 BP. Aleutian artifacts are made out of chopped stone, core, and flake tradition using bifacially carved projectile points. The Aleutian people lived in semisubterranean winter houses made from driftwood, whale bone, and peat. They used kayaks, atlatls and harpoons to kill sea mammals for sustenance. Around 800 BP, there is a shift in lifeways. The Aleutian houses increased considerably in size and food was stored in special chambers. The sustenance pattern changed from relying on sea mammals to eating mostly salmon. Long distance trade also started increasing trade and cultural diffusion with other local groups (Hrdlicka, 1945).
Ales Hrdlicka identified two phenotypes in remains excavated from the Aleutian Island, one he termed Paleo-Aleut, exhibiting a dolichocranic phenotype with little prognathism he linked to artifacts distinguished from later inhabitants, Aleutians, who exhibited a brachycranic phenotype with a greater amount of prognathism (United States National Museum and Hrdlicka, 1944; Hrdlicka, 1945). Hrdlicka suggested a population replacement hypothesis that held Paleo-Aleut's were replaced by Aleutian populations at about 1,000 BP (1945) consistent with the aforementioned shift in lifeway. William Laughlin suggested it was more likely selection for the later craniofacial phenotype or genetic drift that causes this differentiation in the populations (Laughlin and Marsh, 1951). Coltrain et al. (2006) revisiting this research using stable isotope and radiocarbon analysis recently and suggested it is more likely that a population replacement occurred, all materials dating to older than 1,000 BP being Paleoaleut, with a period of coexistence.
It is unclear whether these populations exhibit morphological differences due to population replacement (Hrdlicka, 1945), natural selection for the brachycepahlic phenotype or the influence of genetic drift (Laughlin and Marsh, 1951; Laughlin and Reeder, 1962; Laughlin, 1963, 1975). By comparing patterns of suture synostosis between the Paleo-Aleut and Aleutian may provide some biological information concerning (1) cranial vault phenotype and suture synostosis pattern, and (2) whether these patterns are similar to published norms (Meindl and Lovejoy, 1985), suggesting homogeneity in suture synostosis patterns from Homo sapiens.
MATERIALS AND METHODS
A total of 408 skeletal remains (Umnak-98; Shiprock-101; Kagamil-209) of Paleo-Aleuts and Aleutian as defined by Hrdlicka (1944), housed at the Smithsonian Museum of Natural History, Washington DC, were examined for suture synostosis pattern at a total of 10 ectocranial suture sites: midlambdoid, lambda, obelion, anterior sagittal, bregma, midcoronal, sphenofrontal, pterion, inferior sphenotemporal, and superior sphenotemporal (Meindl and Lovejoy, 1985), Table 1 and Fig. 1. Sites were scored on a scale of 0–3 (0: no closure; 1: 1%–50% closure; 2: 51%–99% closure; 3: complete closure), Fig. 2. Assessments were also performed for sex and age status.
Table 1. Ectocranial suture sites for modal pattern analysis, from Meindl and Lovejoy, 1985
Midlambdoid: midpoint of each half of the lambdoid suture (in pars intermedia” of the lambdoid suture)
Lambda: at lambda (in “pars lambdica” of the sagittal and “pars intermedia” of the lambdoid suture)
Obelion: at obelion (in “pars obelica” of the sagittal suture)
Anterior sagittal: point on the sagittal suture at the juncture of the anterior one third and posterior two-thirds of its length (usually near the junction of the “pars bregmatica” and “pars verticis” of the sagittal suture)
Bregma: at bregma (in “pars bregmatica” of the coronal and “pars bregmatica” of the coronal suture)
Midcoronal: midpoint of each half of the coronal suture (in “pars complicate” of the coronal suture)
Pterion: at pterion, the region of the upper portion of the greater wing of the sphenoid, usually the point at which the parietosphenoid suture meets the frontal bone
Sphenofrontal: midpoint of the sphenofrontal suture
Inferior sphenotemporal: point of the sphenotemporal suture lying at its intersection with a line connecting both articular tubercles of the temporomendibular joint
Superior sphenotemporal: point on the sphenotemporal suture lying 2 cm below its juncture with the parietal bone
Materials were culled by eliminating those that lacked a cranium, exhibited no suture fusion or complete calvarial suture fusion, or damage preventing analysis. A total of 212 total crania were included in the analysis (Male 44%, Female 40%, Unknown 16%; 80% Adult, 20% Subadult).
Modal patterns of commencement and termination of suture activity (progression), osteoblastic and osteoclastic activity that results in bone formation across the fibrous joint, were investigated for lateral-anterior suture sites (sphenofrontal, inferior sphenotemporal, superior sphenotemporal, pterion, and midcoronal) and vault suture sites (midlambdoid, lambda, obelion, anterior sagittal, bregma, midcoronal, and pterion). Commencement of suture fusion was defined as the earliest onset of bone formation activity within the fibrous joint. Termination of suture fusion was defined as the cessation of that activity or synostosis, that is, the fibrous joint is replaced by bone (Meindl and Lovejoy, 1985; Cray et al., 2008).
Guttman scaling was used to determine the most commonly occurring patterns of ectocranial suture synostosis for commencement and termination, for those remains identified as Aleut, Paleo-Aleut, and the collection combined. These results were compared with published standards for Homo sapiens ectocranial suture fusion progression (Table 2) (Meindl and Lovejoy, 1985; Cray et al., 2008, 2010). The Guttman approach assesses the likelihood of unidimensionality, a notion best assessed by the summary measure, CR, the coefficient of reproducibility. This coefficient is reduced by the number of abmodal specimens and measures the strength and validity of a unidimensional cumulative scale. Abmodal patterns are orderings of synostosis that differ in some way from the most commonly occurring pattern. However, scores that approach 1.00 suggest the existence of a single pattern of synostosis and only a small fraction of minor deviations. The coefficient of reproducibility also can be understood in terms of seriation and observer error. The higher the coefficient of reproducibility, the fewer abmodal patterns exist, the greater the preponderance of a single continuum, and the more useful that the crania can be in seriation by the observer to determine relative biological age (Meindl and Lovejoy, 1985; Cray et al., 2008).
Table 2. Modal patterns of ectocranial suture closure for Homo sapiens, from Meindl and Lovejoy, 1985
Tables 3–5 illustrate the results of the scalar analyses. All analyses represent true Guttman scales and high coefficients of reproducibility (> 0.85) indicating largely unidimensional scales. Results for Guttman analyses of the overall collection pattern, Aleut, and Paleo-Aleut, and each island suggests a similar pattern of ectocranial suture synostosis for the two populations. For vault suture commencement, there does not appear to be a strong directional pattern of fusion. For vault suture termination, early fusion activity does appear at the sagittal suture sites in both the Pre-Aleut and Aleut (Tables 3 and 4). This is also consistent with the published standard (Table 2). For lateral-anterior commencement, there appears to be a superior to inferior pattern of fusion for both the Aleut and Pre-Aleut. For lateral-anterior termination, Aleut and Pre-Aleut demonstrate the same pattern, with midcoronal site terminating fusion later in sequence compared with the early commencement observed for this site.
Table 3. Modal patterns of ectocranial suture closure for Paleo-Aleutian affinity
A combined data set (Table 5) is best for evaluation due to little derivation in patterns for these populations and strong Guttmann scales. This combined pattern differs slightly from published standards (Table 2). For vault commencement, the combined Aleutian derivate in midcoronal and midlambdoid sites commencing fusion earlier in the ontogeny sequence with sagittal sites commencing later. For lateral-anterior commencement, pterion comes later in the ontogeny for the combined Aleutians. For vault termination, pterion comes earlier in ontogeny for the combined Aleutians.
The Aleutian and Paleo-Aleutian patterns from the Aleutian island collections did not demonstrate strong differences in patterns of suture fusion. In addition, all scales exhibited strong reproducibility statistics suggesting homogeneity. Overall, the lateral-anterior patterns of suture fusion were most homogenous, compared with the vault suture patterns within the Aleutian populations, similar to standards reported for Homo sapiens (Meindl and Lovejoy, 1985), and other Hominoids (Cray et al., 2008, 2010). The suture synostosis patterns reported here, although similar, differ slightly compared with standards reported in the literature (Meindl and Lovejoy, 1985). The strongest evidence for a suture pattern difference can be observed for the modal commencement scales. This observation suggests that suture fusion patterns may be population dependent and can affect palaeodemographic and forensic analysis utilizing methods of assessing suture fusion.
There was no consistent pattern of earlier sagittal suture site fusion for the dolicocephalic population or coronal suture sites for the brachycephalic populations. Thus, these results suggest suture synostosis pattern is independent of head shape within Homo sapiens populations. This is contrary to that observed in early suture fusion, craniosynostoses, which exhibit cranial shapes determined by the growth trajectories of the fused suture (Babler and Persing, 1982; Enlow and Hans, 1996; Cohen and MacLean, 2000; Cohen, 2005).
These data provide further evidence that the final shape of the cranium is most likely influenced by early expansion of the brain (Weidenreich, 1941; Moss and Young, 1960; Moss and Salentijn, 1969; Enlow and Hans, 1996; Mooney et al., 2002; Richtsmeier et al., 2006). We observed no difference in pattern of suture fusion by cranial shape, brachy vs. dolicocranic. The patterns of suture fusion (i.e., the bridging of bone across the cranial suture) may be more reflective of the functional relationship between patterns of suture fusion and biomechanical stresses and strains due to forces such as mastication (Byron et al., 2004, 2006, 2008; Vecchione et al., 2007, 2010). There is a wealth of experimental research suggesting masticatory biomechanical forces increase sutural adaptations including interdigitation and eventual fusion (Moss and Young, 1960; Riesenfeld, 1967b; Herring, 1972, 1993; Byron et al., 2004; Sun et al., 2004; Shibazaki et al., 2007; Wu et al., 2007; Herring, 2008). Calvarial sutures respond to strains through bony growth and remodeling at the osteogenic fronts (Herring and Teng, 2000; Mao, 2002; Fong et al., 2003; Alaqeel et al., 2006; Wu et al., 2007; Herring, 2008). The calvarial sutures also respond to strain by increasing complexities, waveform patterns, and interdigitations and maintain a relatively constant width by bony adaptation to strain before osseous fusion (Byron et al., 2004, 2006, 2008; Byron, 2006; Yu et al., 2009).
This outcome, a lack of association between cranial shape and patterns of suture fusion, is not unexpected given the temporal disassociation between cessation of neurocranial expansion and growth, which precedes cranial suture remodeling and fusion (Meindl and Lovejoy, 1985; Cohen and MacLean, 2000). However, both cranial shape and suture synostosis pattern may be influenced by similar variables, such as diet, at different times in ontogeny. Thus, it is unknown whether suture patterns or cranial shape is a better measure of heritability in intrapopulation and/or inter population variability, as these variables appear independent of one another.
Results reported here suggest (1) suture synostosis patterns in normal ontogeny are independent of cranial shape and (2) suture synostosis pattern may be population dependent and may affect palaeodemographic and forensic analysis utilizing methods of assessing suture synostosis. Research is still necessary to address questions of why sutures fuse, abstracting suture pattern data to address population relatedness, and the mechanism of suture fusion should continue to be explored.
The authors thank Dr. David Hunt of the Smithsonian Museum of Natural History for access to study specimens.