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Ectocranial Suture Closure in Pan Troglodytes and Gorilla Gorilla: Pattern and Phylogeny James Cray Jr.,1* Richard S

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Ectocranial Suture Closure in Pan Troglodytes and Gorilla Gorilla: Pattern and Phylogeny James Cray Jr.,1* Richard S AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 136:394–399 (2008) Ectocranial Suture Closure in Pan troglodytes and Gorilla gorilla: Pattern and Phylogeny James Cray Jr.,1* Richard S. Meindl,2 Chet C. Sherwood,3 and C. Owen Lovejoy2 1Department of Anthropology, University of Pittsburgh, Pittsburgh, PA 15260 2Department of Anthropology and Division of Biomedical Sciences, Kent State University, Kent, OH 44242 3Department of Anthropology, The George Washington University, Washington, DC 20052 KEY WORDS cranial suture; synostosis; variation; phylogeny; Guttman analysis ABSTRACT The order in which ectocranial sutures than either does with G. gorilla, we hypothesized that this undergo fusion displays species-specific variation among phylogenetic relationship would be reflected in the suture primates. However, the precise relationship between suture closure patterns of these three taxa. Results indicated that closure and phylogenetic affinities is poorly understood. In while all three species do share a similar lateral-anterior this study, we used Guttman Scaling to determine if the closure pattern, G. gorilla exhibits a unique vault pattern, modal progression of suture closure differs among Homo which, unlike humans and P. troglodyte s, follows a strong sapiens, Pan troglodytes,andGorilla gorilla.BecauseDNA posterior-to-anterior gradient. P. troglodytes is therefore sequence homologies strongly suggest that P. tr og lodytes more like Homo sapiens in suture synostosis. Am J Phys and Homo sapiens share a more recent common ancestor Anthropol 136:394–399, 2008. VC 2008 Wiley-Liss, Inc. The biological basis of suture synostosis is currently Morriss-Kay et al. (2001) found that maintenance of pro- poorly understood, but appears to be influenced by a liferating osteogenic stem cells at the margins of mem- combination of vascular, hormonal, genetic, mechanical, brane bones forming the coronal suture requires FGF and local factors (see review in Cohen, 1993). A primary levels to be relatively low, while higher levels of FGF are goal of suture biology research is to investigate what associated with osteogenic differentiation. In the normal causes craniosynostosis. This has shed some light on the suture, this mechanism involves differential levels of processes of normal sutural fusion and the roles of trans- FGF, from high in the differentiated region to low in the forming growth factors (TGFb) and fibroblast growth fac- suture, and is thought to ensure that sutural stem cell tors (FGF). Cohen and others have argued (Cohen and populations are maintained at the periphery of growing MacLean, 2000; Law et al., 2005) that a suite of growth bones. However, when receptor activation is increased, factors interact to regulate suture morphogenesis, pat- either experimentally, or pathologically, FGFR2is ency, and eventual fusion, and recent studies of patho- prematurely down-regulated and proliferation ceases logical craniosynostosis have consistently demonstrated (Morriss-Kay et al., 2001). Bone morphogenetic proteins that premature fusion can result from failure of either (BMP), MSX2, Twist, and RUNX2/Cbfa1, also all appear up-regulation or down-regulation of genetic signaling to be necessary for normal suture morphogenesis and (Morriss-Kay and Wilkie, 2005). Suture closure is seen the regulation of suture patency (Kim et al., 1998; to proceed largely by genetic mechanisms, especially Opperman and Ogle, 2002). those involving the expression of FGFs and their recep- There is no current agreement on the functional rela- tors (FGFRs) as well as TGFb. The TGFbs (1, 2, and 3) tionship between strain and suture morphology or its have been shown to regulate suture patency by regulat- effect on suture morphology. Some have argued that ing cell proliferation and apoptosis among those cells mechanical forces are too small in magnitude to affect within the articulating bone fronts (Opperman and Ogle, suture morphology (Henderson et al., 2004). In support 2002). of this conclusion, Sun et al. (2004) observed that me- The FGF signaling pathway is highly conserved in chanical forces generated by chewing in pigs do not cor- evolution and appears to play a crucial role in develop- relate with sutural strain magnitude. However, these ment and early patterning of the entire craniofacial authors did suggest that fusion of the interfrontal suture region. It is likely important in suture and synchondro- in their model was associated with increased strain and sis regulation (Carinci et al., 2002; Nie et al., 2006, Ogle ectocranial surface growth. Other investigators have con- et al., 2004). Patency and growth are believed to be cluded that there is a positive functional relationship maintained by inductive interaction with the underlying dura mater and its FGFs (Alden et al., 1999, Kim et al. *Correspondence to: James Cray Jr., Department of Anthropology, 1998), although this model has been called into question University of Pittsburgh, 3302 Posvar Hall, Pittsburgh, PA 15260, (Mooney et al., 2001). Specifically FGF2, localized to the USA. E-mail: [email protected] underlying dura mater, becomes highly expressed in the osteogenic bone fronts of fusing sutures (Opperman and Received 3 September 2007; accepted 24 January 2008 Ogle, 2002). Basic fibroblast growth factor (bFGF) expression is increased in the dura just prior to suture DOI 10.1002/ajpa.20821 fusion, and by increased expression in osteoblasts sur- Published online 18 March 2008 in Wiley InterScience rounding the suture during fusion (Alden et al., 1999). (www.interscience.wiley.com). VC 2008 WILEY-LISS, INC. HOMINOID ECTOCRANIAL SUTURE CLOSURE 395 between masticatory muscle force and sutural complex- ity, evidenced by sutural interdigitation (Byron et al., 2004, 2006, Fong et al., 2003). Kopher and Mao (2003) suggest that cyclic compressive forces, e.g., chewing ac- tivity, increase bone deposition at sutural margins. Wu et al. (2007) suggest that suture complexity is directly influenced by environmental factors, and variation seen in the complexity of human sutures is directly due to Fig. 1. Suture closure stages. Illustration of a suture site that influence, owing to little genomic variation. Age has scored as a 0 or no observable closure and a site scored 1 or 1– also been shown to have an impact on suture morphol- 50% closure. University of Pittsburgh, Department of Anthro- ogy (Byron et al., 2004). It is possible that sutures pology, Comparative Anatomy Collection. respond to increased strain by upregulating activity of extracellular matrix proteins (Opperman and Rawlings, ensic ageing study in modern humans. They employed 2005), but this relationship has not been well studied. 10 such sites, determined a modal pattern of closure, Most recently, an experimental study associating rat cal- and noted four primary observations with respect to varial bone morphology and biomechanical strain both initiation and commencement: 1) closure in the lat- showed no influence on the fusion of the interfrontal eral-anterior (i.e., ‘‘circum-meatal’’) sutures follows an suture or patency of the sagittal suture with increased anterior-to-posterior pattern; 2) final closure of the lat- biomechanical strain (Shibazaki et al., 2007). eral-anterior sites also follows this pattern; 3) the sagit- Sutural architecture, growth, and eventual fusion is tal suture commences closure before the lambdoid and very likely the result of several complex factors, includ- coronal; and 4) the sagittal suture is first to complete ing gene expression and epigenetic factors including closure along its middle section (at obelion), is followed, environmental factors such as compressive and tensile in sequence, by closure at bregma and lambda, and forces causing mechanical signaling, activity of local cell finally by closure of the inferior portions of the coronal populations, and cytokines, as well as hormones (Cohen and lambdoid. and Maclean, 2000; Mooney and Richtsmeier, in press). The methods used by Meindl and Lovejoy to determine The apparent disassociation in humans and perhaps the modal patterns of closure for humans can be used to their closest living relatives (Pan and Gorilla) between determine patterns of other species. Because sutural brain growth and suture activity complicates the issue synostosis should contain phylogenetic information, it and suggests that mechanical factors, specifically the would be useful to apply these methods and to revisit growing brain, is not solely responsible for the onset of Krogman’s findings to determine the modal sequence of suture architecture, growth, and fusion. The question closure for G. gorilla and P. troglodytes, and to describe still remains whether gene responses within the cell are potential differences between these species. Description responsible for the final morphology of the suture are of this variation is a major goal of the present research. mediated by morphogenetic or paracrine signals, or In addition, this may also provide a better understand- whether they are generated by mechanical stimulation. ing of functional and developmental implications of suture biology, including the role of genetics in the spe- The use of suture closure patterns to deduce cies studied here, and the role that functional influences phylogenetic information may play in variations of suture morphology. With the exception of some rare genetic disorders of MATERIALS AND METHODS cranial growth, sutural synostosis is very likely largely a genetic trait that should contain substantial phyloge- Samples comprising 381 G. gorilla (56.4%
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