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Paschetta Et Al 2010C.Pdf AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 141:297–314 (2010) The Influence of Masticatory Loading on Craniofacial Morphology: A Test Case Across Technological Transitions in the Ohio Valley Carolina Paschetta,1 Soledad de Azevedo,1 Lucı´a Castillo,2 Neus Martı´nez-Abadı´as,3 Miquel Herna´ ndez,3 Daniel E. Lieberman,4* and Rolando Gonza´ lez-Jose´ 1* 1Centro Nacional Patago´nico, Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas (CONICET), U9120ACD, Puerto Madryn, Argentina 2Universidad Nacional de la Patagonia San Juan Bosco, 9120, Puerto Madryn, Argentina 3Unitat d’Antropologia, Departament de Biologia Animal, Universitat de Barcelona. 08028 Barcelona, Spain 4Peabody Museum, Harvard University, Cambridge, MA 02138 KEY WORDS masticatory stress; upper-middle Ohio valley; skull shape; geometric-morphometrics; technological transition ABSTRACT Masticatory loading is one of the main and food processing technology. Geometric morphometric environmental stimuli that generate craniofacial variation methods were used to detect and measure the putative among recent humans. Experimental studies on a wide effect of diet changes on cranial shape independent of variety of mammals, including those with retrognathic size. Our results partially confirm only some of the exper- postcanine teeth, predict that responses to masticatory imental predictions. The effect of softer and/or less tough loading will be greater in the occlusal plane, the inferior diets on craniofacial shape seem to be concentrated in the rostrum, and regions associated with the attachments of relative reduction of the temporal fossa and in a displace- the temporalis and masseter muscles. Here we test these ment of the attachment of the temporal muscle. However, experimentally-derived predictions on an extinct human there were few differences in craniofacial shape in regions population from the middle and upper Ohio valley that closer to the occlusal plane. These results highlight the underwent a marked shift from hunting-gathering to utility of exploring specific localized morphological shifts extensive farming during the last 3,000 years and for using a hierarchical model of craniofacial integration. Am which we have good archaeological evidence about diet J Phys Anthropol 141:297–314, 2010. VC 2009 Wiley-Liss, Inc. The adult form of complex phenotypes, such as craniofa- (Carlson and Van Gerven, 1977), an increase in temporal cial size and shape, derives from multiple, intricate devel- muscle area (Carlson, 1976; Carlson and Van Gerven, opmental processes that are affected by both genetic and 1977; Gonza´lez-Jose´ et al., 2005; Sardi et al., 2006), an epigenetic stimuli (Cheverud, 1988; Enlow, 1990; Atchley increase in temporo-mandibular joint size (Hinton and and Hall, 1991; Wagner, 1996; Wagner and Altenberg, Carlson, 1979; Corruccini and Handler, 1980) and an 1996; Hallgrimsson et al., 2002, 2004; Lieberman et al., increase in the cranial vault thickness (Hylander, 1986; 2002; Klingenberg et al., 2003; Gonza´lez-Jose´ et al., 2004). Lieberman, 1996). Even though there is evidence supporting genetic deter- minism on craniofacial form (Martı´nez-Abadı´as et al., 2009), there is a general appreciation that epigenetic stim- uli play a major role in influencing overall skull shape Grant sponsor: Ministerio de Educacio´nyCiencia;Grantnumber: CGL2004-00903/BTE; Grant sponsor: Agencia Nacional para la both from interactions within the organism (e.g., pattern- Promocio´n Cientı´fica y Tecnolo´gica (project PICT Jo´venes 2004), ing of migrating neural crests cells as they come into con- Argentina; Grant number: 20582; Grant sponsor: FEDER (Fondos tact with mesoderm) as well as from environmental stim- Europeos de Desarrollo Regional), Spain. uli (see Beecher and Corruccini, 1981; Hallgrimsson et al., 2007a,b). Among the many environmental factors that Present address of Neus Martı´nez-Abadı´as: Department of may have influenced the evolution of the highly derived Anthropology, Penn State University, 409 Carpenter Building, Uni- human face, masticatory loading in response to variations versity Park, PA 16802. in hardness, toughness, and particle size in diet is thought to be particularly important (Corruccini and Handler, *Correspondence to: Rolando Gonza´lez-Jose´, Centro Nacional Patago´nico, Bvd. Brown 2915, U9120ACD, Puerto Madryn, 1980; Beecher and Corruccini, 1981; Corruccini and Argentina. E-mail: [email protected] or Daniel E. Lieberman, Beecher, 1982, 1984; Beecher et al., 1983; Corruccini et Peabody Museum, Harvard University, 11 Divinity Avenue, Cam- al., 1985; Ingervall and Bitsanis, 1987; Larsen, 1995, bridge, MA 02138, USA. E-mail: [email protected] 1997; Ciochon et al., 1997; Corruccini, 1999; Lieberman et al., 2004; Gonza´lez-Jose´ et al., 2005; Lieberman, 2008). Received 13 November 2008; accepted 1 July 2009 Previous studies agree that hard, tough and/or unpro- cessed diets generally lead to an increase in the overall DOI 10.1002/ajpa.21151 robusticity (Larsen, 1995, 1997), or size (Sardi et al., 2006) Published online 9 November 2009 in Wiley InterScience of the skull, an increase in facial size relative to total size (www.interscience.wiley.com). VC 2009 WILEY-LISS, INC. 298 C. PASCHETTA ET AL. Since hard nonprocessed diets are the ancestral condi- One of the advantages of experimental studies is the tion prior to the invention of cooking and other food ability to control for the effect of alternative sources of processing technologies, some degree of craniofacial environmental and genetic variation that clearly play an change is expected to result from technological changes important role in natural populations. However, natural over the last few thousand of years that have permitted populations are subject to an unknown number of differ- humans to eat softer, less tough, and more processed ent environmental stimuli which act simultaneously and foods. In particular, it is frequently assumed that a in an integrated fashion on cranial growth and develop- reduction in masticatory muscle activity and a concomi- ment. For instance, among most hunter-gatherers hard- tant decrease in mechanical loading of the craniofacial ness and toughness of the diet is usually accompanied skeleton are responsible for a reduction in muscle size by varying levels of abrasiveness. Moreover, parafunc- and their related structures. Further, because mechani- tional dental use is ubiquitous among hunter-gatherer cal strains induce bone growth, especially prior to skele- populations. Obviously, sex and age contribute further tal maturity (for review, see Pearson and Lieberman, sources of uncontrolled variation. In summary, 2004), and because chewing harder and tougher foods classifying diets as ‘‘hard’’ versus ‘‘soft’’ or ‘‘processed’’ generates higher strains in the lower face (see below), versus ‘‘unprocessed’’ in natural human populations less processed diets should lead to relatively more cra- oversimplifies a complex array of masticatory stimuli niofacial growth in the mandible, lower maxilla, and influenced by many parameters such as hardness, tough- other regions subject to greater loading (for review, see ness, particle size, as well as other factors such as age of Wood and Lieberman, 2001). In this context, technologi- weaning, abrasives in the diet, paramasticatory loading, cal changes related to the shift from hunting-gathering and so on. In summary, there is a strong need to comple- or foraging to food production and cooking, as well as ment experimental studies of the effects of masticatory the incorporation of softer foods are hypothesized to loading with comparative analyses of natural popula- have led to reduced masticatory activity and the concom- tions. itant gracilization trend observed among recent humans There have been several previous comparative studies (Carlson, 1976; Carlson and Van Gerven, 1977; Brace of craniofacial shape in populations that ate different et al., 1987; Hannam and Wood, 1989 ; Brace et al., diets (Carlson, 1976; Carlson and Van Gerven, 1977; 1991; van Spronsen et al., 1991; Kiliaridis, 1995; Larsen, Hinton and Carlson, 1979; Corruccini and Handler, 1995, 1997; Lieberman et al., 2004; Sardi et al., 2006; 1980; Corruccini et al., 1985; Brace et al., 1987, 1991; Pinhasi et al., 2008). Larsen, 1997; Gonza´lez-Jose´ et al., 2005; Sardi et al., Although the importance of mechanical loading on 2006; Pinhasi et al., 2008). Most of these studies focus facial growth is well appreciated, how the face is loaded on comparisons between hunter-gatherers and farmers, during mastication is only partially understood, espe- taking advantage of the general assumption that cially in the human face, which is highly derived relative technological advances in the preparation of food that to other primates in several respects such as the pres- accompanied the origin of agriculture led to decreases in ence of a retrognathic face, and a reorientation and hardness and toughness in the diet of farmers versus expansion of the surface of the face in the coronal plane foragers. This assumption is generally corroborated by (Lieberman et al., 2004). Nevertheless, experiments on a evidence that hunter-gatherers typically have larger and wide variety of nonhuman primates and other mammals more robust skulls (Brace et al., 1987, 1991; Larsen, permit several reliable inferences. First, mastication 1995, 1997; Sardi et al., 2006). Larsen (1995), for generates a gradient of strains in the face with highest instance, suggests that gracilization of the skull is a strains
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