Craniofacial morphology in the Argentine center-west Consequences of the transition to food production.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 130:333–343 (2006) Craniofacial Morphology in the Argentine Center-West: Consequences of the Transition to Food Production Marina L. Sardi,1,2* Paula S. Novellino,2,3 and Héctor M. Pucciarelli1,2 1 Departamento Cientı́ﬁco de Antropologı́a, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, 1900 La Plata, Argentina 2 Consejo Nacional de Investigaciones Cientı́ﬁcas y Técnicas, Buenos Aires, Argentina 3 Laboratorio de Bioarqueologı́a, Museo de Historia Natural de San Rafael, 5600 San Rafael, Mendoza, Argentina KEY WORDS subsistence economy; functional cranial components; masticatory stress ABSTRACT The Argentine Center-West was the southernmost portion of the Andes where domestication of plants and animals evolved. Populations located in the southern portion of this area displayed a hunter-gatherer subsistence economy up to historical times, and coexisted with farmers located to the north. Archaeological and biological evidence suggests that the transition to food production was associated with the consumption of a softer diet and a more sedentary way of life. This study tests the hypothesis that diet-related factors inﬂuenced morphological differentiation, by comparing functional cranial components of farmers and hunter-gatherers. Three-dimensional changes on eight minor functional components (anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory, and alveolar) were measured on skulls derived from both subareas. Volumetric and morphometric indices were calculated to estimate the absolute and relative size of components, respectively. Results of a paired t-test indicated that farmers have a smaller craniofacial size than hunter-gatherers. The components that varied the most were masticatory and posteroneural, showing smaller absolute and relative sizes in farmers. Discriminant analyses indicated that lengths and widths were the most affected dimensions of these and other components. The pattern of differentiation, which involves speciﬁc components, enabled us to exclude differential gene ﬂow and stochastic mechanisms as the main causes. Instead, results support the hypothesis that diet-related factors associated with both subsistence economies inﬂuenced craniofacial morphology. A proportion of the observed variation associated with size differences can be explained by two systemic factors: the lesser quality of nutrition due to a low protein content in the diet, and a decrease of growth hormone circulation induced by a lower mobility due to sedentism. However, differentiation is better explained by a localized factor: the reduction in the masticatory and posteroneural components in farmers resulted from a decrease of masticatory stresses and workload on the head and neck, linked to the consumption of a softer diet. Am J Phys Anthropol 130:333–343, 2006. V 2006 Wiley-Liss, Inc. One of the most important changes in human evolution during the Holocene was the transition from hunting and gathering to food production. The increased dependence on agriculture and pastoralism implied several transformations of biological characteristics in human populations worldwide (Pechenkina et al., 2002; Richards, 2002; Larsen, 2003; Eshed et al., 2004). In South America, the earliest evidence of agriculture appeared in Peru and Ecuador, yielding dates of around 6,900 years BP (Pearsall, 1992) or even older (Smith, 1998). The Argentine Center-West was the southernmost portion of the Andes where food production evolved (Gil, 2003). Populations located in the southern portion of this area maintained a hunter-gatherer subsistence economy, coexisting with farmers located in the north. Because morphology arises from the translation of genotype into phenotype through several epigenetic processes, phenotypes of a group of populations express their genetic relationships as well as the inﬂuence of environmental factors acting across ontogeny. Nevertheless, studies are commonly more concerned with distances among populations from a taxonomic point of view than with contextual factors and adaptation (Armelagos and Van Gerven, 2003) that may affect differentiation. Moreover, which structures might be more plastic to these factors is a subject frequently disregarded (GonzálezJosé et al., 2005). BIOCULTURAL CONTEXT C 2006 V WILEY-LISS, INC. C The Argentine Center-West is an archaeological area comprised of the provinces of San Juan and Mendoza (Fig. 1), which are longitudinally variable in geomorphological and ecological terms (Capitanelli, 1972; Roig, 1972; Ruiz Leal, 1972). Three ecological zones can be distinguished: 1) the Andean mountains, with more than 2,000 m of altitude acting as a barrier to humid Paciﬁc winds and promoting arid conditions; 2) a piedmont plateau, between 1,000–2,000-m altitude, which is entirely crossed by valleys, although most of them almost constantly lack water; and 3) plains, at less than 1,000-m altitude. Grant sponsor: Universidad Nacional de La Plata, Argentina; Grant sponsor: Fondation Fyssen, France. *Correspondence to: Marina L. Sardi, Departamento Cientı́ﬁco de Antropologı́a, Museo de La Plata, Paseo del Bosque S/N, 1900 La Plata, Argentina. E-mail: email@example.com Received 3 March 2005; accepted 10 August 2005. DOI 10.1002/ajpa.20379 Published online 18 January 2006 in Wiley InterScience (www.interscience.wiley.com). 334 M.L. SARDI ET AL. Fig. 1. Argentine Center-West. Localities where skulls were recovered. 1, Uspallata; 2, Mendoza; 3, Capiz, 4; Campo Las Julias; 5, Arroyo Imperial; 6, Arroyo El Tigre; 7, Dique Villa 25 (Los Reyunos); 8, Dique Villa 25 (La Hedionda); 9, Dique Villa 25 de Mayo; 10, Los Coroneles; 11, Médano Puerto Dı́az; 12, Arroyo Los Jilgueros; 13, Rincón del Atuel; 14, Loma del Eje; 15, Cañada Seca; 16, Jaime Prats; 17, Cerro Negro; 18, Agua del Médano; 19, El Nihuil; 20, Agua del Zapallo; 21, Cerro Meson; 22, Respolar; 23, La Herradura; 24, Puerto Aisol; 25, El Sosneado; 26, Puerto Tierras Blancas; 27, Cerro Mesa; 28, El Manzano; 29, La Matancilla; 30, El Chacay; 31, La Cañada; 32, Sur de Malargüe; 33, Calingasta; 34, San Juan; 35, Caliningasta Barrealito; 36, Angualasto; 37, Pachimoco; 38, Huaco. In ethnographic and archaeological terms, this area is divided by the Diamante River into northern and southern subareas. The northern subarea comprises the provinces of San Juan and Mendoza up to the Diamante River; the southern subarea is located to the south of Mendoza (Fig. 1). According to ethnohistorical data, aboriginal populations inhabiting the Argentine CenterWest at the arrival of the Spaniards were divided in two different cultural complexes with different subsistence economies. Farmer groups, named Huarpes, inhabited the northern subarea, while the hunter-gatherer Puelches inhabited the southern subarea (Cabrera, 1929; Latcham, 1929; Canals Frau, 1937, 1953; Michieli, 1978; Prieto, 1989; Durán, 1994). Evidence of Late Pleistocene and Early Holocene occupation was dated to 11,000 and 10,500 years BP in the northern and southern subareas, respectively (Gambier, 1976; Garcı́a, 1997; Lagiglia, 2002). Populations based their subsistence on the hunting of guanaco (Lama guanicoe), ñandú (Rhea americana), and other small mammals, and on the gathering of wild plants by seasonal movements between lowlands and highlands (Gambier, 1993; Lagiglia, 2002). The earliest evidence of agriculture in the northern subarea is dated to around 4,400 years BP (Bárcena, 1985), and is associated with pottery and sedentism (Lagiglia, 2002). The transition to food production in the Argentine Center-West was part of a general process that occurred in the South-Central Andean region where, across the archaic cultural tradition, some changes in the archaeological record suggest a diversiﬁcation of diet and a demographic increase (Castro and Tarragó, 1992; Planella and Tagle, 2004). As part of this diversiﬁcation, local groups gradually adopted agriculture and pastoralism, as complementary resources to hunting, gathering, and ﬁshing (Castro and Tarragó, 1992; Gambier, 1993). Potato (Solanum tuberosum), manioc (Manihot esculenta), beans (Phaseolus vulgaris), and maize (Zea mays) were some of the species included in the diet. It is accepted that plant and animal domestication was not a uniform process, but in general terms, a continuity from archaic to formative groups seems to be supported (Castro and Tarragó, 1992; Planella and Tagle, 2004), as occurred in the valleys of northern Chile where continuity was demonstrated by craniometrics and mitochondrial DNA (mtDNA) analyses (Moraga et al., 2005). Some archaeological indicators suggest changes associated with food production in the northern subarea. Grinding-stone artifacts were utilized, and their morphology evidenced food preparation because they were deep and associated with discoid manos (Lagiglia, 1997). Some villages presented collective mills made of large rocks with many pits (Lagiglia, 1997). Pottery remains were diverse (Lagiglia, 2002), and pottery’s use in cooking might enable the boiling of corn and other vegetables as in other Andean populations (Bruhns, 1994). Around 1,500 years BP, agriculture was of primary importance in the economy of the northern group (Gambier, 1993). Settlement patterns changed, revealing the formation of permanent and semipermanent villages. In the northern Mendoza province, the concentration of archaeological assemblages and their association with collective mills suggest an increase in sedentism (Lagiglia, 2002). In San Juan province, the remains of small villages close to river valleys were found, which showed water-control features and dwellings for animals (Gambier, 1993). It is important to state that northern farmers maintained a broad-spectrum diet, with some reliance on hunting and gathering. Nevertheless, at around 1,500 years BP, these activities provided complementary resources, mainly during the winter season (Gambier, 1993). Pastoralism was more important for transport than for food. The use of wild vegetables was reported for the Huarpes, although conﬁned to the preparation of breads and alcoholic drinks (Gambier, 1993). In the southern subarea, groups displayed mobile and seasonal hunting and gathering up to historical times. Cultigens (Zea mays) dated between 1,900–2,200 years BP were found (Hernández, 2002). However, they do not 335 ARGENTINE CRANIOFACIAL DIFFERENTIATION indicate the development of agriculture (Gil, 2002); instead, their caltigens were probably obtained by exchanges with northern populations. Animal domestication was never adopted. Pottery began to be incorporated around 2,000 years BP (Lagiglia, 2002). Flat and small mills were found, but they lack the traces induced by the grinding of grains, which led some authors (Castro and Tarragó, 1992; Lagiglia, 1997) to think that mills were only used for processing pigments. Scrapers (used for skin preparation) are a diagnostic element of habitat occupation, and since they are broadly dispersed, they suggest high mobility and short-term occupations (Lagiglia, 2002). Stable-isotope analyses of human bone (Gil, 2003; Novellino et al., 2004) indicate a small proportion of cultivable plants’ consumption in the southern subarea. Hunter-gatherer skeletons show biological markers of diet (dental wear and presence of caries) and health (porotic hyperosthosis and dental hypoplasia) with a similar pattern to those observed in other hunter-gatherers (Novellino et al., 1996; Novellino, 2002). In contrast, northern farmers show signiﬁcant differences from southern hunter-gatherers due to a higher frequency of caries (Novellino and Guichón, 1997–1998), which may indicate the increased role of carbohydrates in their diet (Larsen, 1995). Hunter-gatherers also show a higher degree of dental wear than farmers, which may indicate the incidence of greater masticatory loads and/or abrasion. These differences in dental wear are most likely due to differences in masticatory stresses, because farmers were also as affected by dental abrasion as huntergatherers due to the inclusion of particles of sand in the food, which was promoted by the use of mills (Lagiglia, 2002). Once the farmers of the Argentine Center-West acquired new techniques of cooking, such as grinding and boiling with the use of mills and pottery, which was a common practice among farmers of the Andean region (Bruhns, 1994), they consumed a softer diet than hunter-gatherers. THE FUNCTIONAL PARADIGM IN CRANIOFACIAL STUDIES In the 1960s, the ‘‘functional paradigm’’ appeared in the study of craniofacial growth, in opposition to the ‘‘genomic paradigm’’ that pointed out the preeminence of genes in the expression of growth patterns (Carlson, 1999). The paradigm was developed by Melvin Moss, who postulated the functional matrix hypothesis (Moss, 1973, 1997a–c), which states that cranial shape reﬂects its primary functions of support and protection of the related functional tissues and spaces (Moss and Young, 1960). Each function of the head, such as digestion and vision, is performed by a functional cranial component comprised of the functional matrix and the skeletal unit (Moss, 1973; Carlson, 1999). All soft tissues, organs, and cavities necessary to carry out a function comprise the functional matrix, classiﬁed as: 1) periosteal matrix (muscles and neurovascular structures of the direct functional environment), and 2) capsular matrix (cavities and larger organs such as the brain and eyes). The group of hard tissues (bone and cartilage) and others (tendon and ligaments) that give biomechanical support to the functional matrix comprises the skeletal unit, classiﬁed as: 1) the microskeletal unit, which expresses the constraints made by the periosteal matrix, such as tuberosities or ridges for muscle attachment; and 2) the TABLE 1. Samples derived from Argentine Center-West Females, n (%) Males, n (%) Farmers not deformed Farmers deformed 13 (10.5) 20 (16.1) 7 (5.6) 18 (14.5) Hunter-gatherers not deformed Hunter-gatherers deformed Total 18 (14.5) 31 (25.0) 5 (4.0) 12 (9.6) 56 (45.1) 68 (54.8) Total, n (%) 20 38 58 49 (16.1) (30.6) (46.7) (39.5) 17 (13.7) 66 (53.2) 124 (100) macroskeletal unit, which expresses the constraints made by the capsular matrix and associated skeletal structures. The functional matrix hypothesis proposes that bone does not regulate the rate and direction of its growth by means of its own genetic control. Instead, bone is epigenetically modiﬁed by the growth of the functional matrix associated with it (Moss, 1973, 1997c). Thus, each component is relatively independent in form (size and shape) and spatial position (Moss and Simon, 1968). Due to the particular association of functional matrices and skeletal units, components can be classiﬁed as: 1) contiguous (a single skeletal structure and different functional matrices, such as the mandible), and 2) adjacent (different skeletal structures associated with the same functional matrix, such as the zygomatic arch and the mandibular angle) (Moss and Simon, 1968). Hunter-gatherers and farmers of the Argentine Center-West might differ in craniofacial morphology. Differences could evolve due to environmental factors, stochastic mechanisms, and differential gene ﬂow with populations from outside the Argentine Center-West. Among environmental factors, the subsistence economy is the most important, since geography and ecology throughout the northern and southern subareas are quite similar. Biological consequences of the transition to food production are usually attributed to a decline in the quality of nutrition and reduction in workload (Cohen and Armelagos, 1984; Ruff et al., 1984; Ruff, 1987; Larsen, 1995). The effect of diet-related factors on craniofacial structures was demonstrated by comparative (e.g., Carlson and Van Gerven, 1979; Hinton, 1983; Varrela, 1992; Kaifu, 1997; Sardi et al., 2004) and experimental (e.g., Beecher et al., 1983; Lieberman et al., 2004) analyses. A general hypothesis to be tested in this study is that diet-related factors intervene in the differentiation of farmers and huntergatherers of the Argentine Center-West. If this is true, differentiation should not be stochastically distributed throughout the skull. Instead, it should involve speciﬁc functional components, mainly those that participate in mastication and reﬂect differences in workload on the skull due to differences in food consistency. MATERIALS AND METHODS Samples Adult skulls of both sexes, derived from northern and southern subareas of the Argentine Center-West, were analyzed (Table 1, Fig. 1). The material is housed at the Museo de Historia Natural (San Rafael), Museo Etnográﬁco (Buenos Aires), and Museo de La Plata (La Plata) in Argentina. All individuals present closure of the sphenooccipital synchondrosis (Buikstra and Ubelaker, 1994). 336 M.L. SARDI ET AL. TABLE 2. Functional matrix of components and interlandmark measurements1 Component Functional matrix Anteroneural Neural structures related to anterior cranial fossa (mainly anterior lobes) Midneural Neural structures related to middle and part of posterior cranial fossae and most parts of brain hemispheres Cerebellum Posteroneural Otic Bones and organs for hearing and equilibrium Optic Ocular globe Respiratory Cavity for respiration and smell Masticatory Temporal and part of masseter muscles Alveolar Teeth and tissues of oral cavity Interlandmarks measurements L: glabella-bregma2 W: pterion-pterion H: bregma-hormion L: bregma-lambda2 W: eurion-eurion H: basion-bregma L: opisthion-opisthocranium2 W: asterion-asterion H: lambda-opisthion2 L: posterior-inferior limit of tympanic bone, to midpoint of inner extreme of petrous bone W: external auditive meatus width2 H: external auditive meatus height2 L: dacryon-optic foramen W: dacryon-ectoconchion H: midpoint of supraorbitary border to midpoint of infraorbitary border L: subspinale-posterior nasal spine W: widest extension of anterior nasal aperture H: nasion-subspinale L: zygomaxillare-posterior border of glenoid cavity2 W: anterior sulcus of sphenotemporal crest-lower point of zygotemporal synchondrosis2 H: lower border of zygotemporal synchondrosis-upper temporal line at coronal intersection2 L: external prosthion-posterior alveolar border2 W: from left to right alveolar borders, at unions between second and third molars H: intermaxillary synchondrosis-alveolar border, at unions between second and third molars2 1 L, length; W, width; H, height. Projected measurements. They must be done in relation to auricular-infraorbitary equalization (Frankfurt plane). In contrast, direct measurements may be made out of Frankfurt orientation. 2 Sex determinations were done on the pelvis and skull, following the standards described by Buikstra and Ubelaker (1994): ventral arch, subpubic concavity, ischiopubic ramus ridge, sciatic notch, preauricular sulcus (on the pelvis), nuchal crest, mastoid process, supraorbital margin, and glabellar and mental eminences (on the skull). The sample from the southern subarea is represented by 66 adult skulls. Seventeen individuals present occipital artiﬁcial deformation (Table 1). Individuals were found in three ecological zones: mountains (n ¼ 3), piedmont (n ¼ 4), and plains (n ¼ 59) (Fig. 1). Thirty-ﬁve percent of the sample was provided by the ‘‘Jaime Prats’’ cemetery, with two dates at 2,040 6 120 and 1,755 6 80 years BP (Novellino and Guichón, 1999). Archaeological assemblages of the whole sample express that individuals displayed a mobile hunter-gatherer economy. For at least half of the sample, assemblages do not include pottery (Novellino et al., 1996). The sample derived from the northern subarea is represented by 58 skulls. Among them, 38 individuals present occipital and front-occipital deformation (Table 1). They were recovered from localities in mountains (n ¼ 43), piedmont (n ¼ 8), and plains (n ¼ 7) (Fig. 1). There are no radiocarbon dates associated with this material; thus, chronology was inferred through archaeological indicators, such as pottery, dwellings, and the presence of irrigation systems. They can most likely be assigned to the Late Agriculturalist period (500–800 BP) (Gambier, 1993) and to the ethnographic Huarpes (Lehmann Nitsche, 1910). A third sample was added as a reference to measure internal variation of samples of the Argentine Center- West. These individuals of known age and sex derive from a cemetery in the city of Coimbra (Portugal), born during the last part of the 19th century and studied by Rosas and Bastir (2002), Albanese (2003), and Sardi and Ramı́rez Rozzi (2005), among others. The sample comprises 102 females and 100 males of Portuguese origin, between 18–39 years of age, with closure of the sphenooccipital synchondrosis. They are housed at the Museu Antropologico of Coimbra (Coimbra, Portugal). Craniometric method The morphological assessment was based on the functional matrix hypothesis, as applied in previous studies (Pucciarelli et al., 1990; Sardi et al., 2004; González-José et al., 2005). The neurocranium and face are major components of the skull. The neurocranium was divided into four functional components: anteroneural, midneural, posteroneural, and otic. Another four comprise the face: optic, respiratory, masticatory, and alveolar (Table 2). Length, width, and height were measured for each component with spreading, sliding, coordinate, and Poech calipers. In this method, no component is over- or underrepresented because each has the same quantity of measurements, expressing three-dimensional changes which render the method sensitive to more aspects of cranial variation (O’Higgins, 1989). Another property of the method is that interlandmark measurements do not overlap among them. Thus, the correlation matrix of measurements represents ‘‘organic’’ correlations, because it measures associations between different cranial regions, ARGENTINE CRANIOFACIAL DIFFERENTIATION 337 TABLE 3. Methods for estimating absolute and relative size of components Indices Volumetric (VI) Neural morphometric Facial morphometric Difference between means Equation p 3ﬃ (length 3 breadth 3 height) Neural VI/SVI anteroneural, midneural, posteroneural, and otic Facial VI/SVI optic, respiratory, masticatory, and alveolar (Mean of hunter-gatherers’ VI mean of farmers’ VI)/[(mean of hunter-gatherers’ VI þ mean of farmers’ VI)/2] rather than ‘‘spurious’’ correlations which reﬂect redundant measurements of the same structure (Armelagos and Van Gerven, 2003). Moreover, since different functional matrices have relatively independent embryological origins and growth patterns, speciﬁc coordinates should measure them. This method is more suitable than the macromeasurements commonly used in biological anthropology to identify which region shows the greatest amount of variation. Data analyses Assessment of within-samples variation. Since some factors like sex and deformation can inﬂate variance within samples, contingency tables were constructed to evaluate if dependency existed among these factors. Another factor that inﬂates variances is artiﬁcial deformation, which also affects morphology (Anton, 1989), even in those structures that do not undergo deformation directly (Anton and Weinstein, 1999). To test whether deformation had an inﬂuence or not on within-samples variation, linear measurements of each component were compared after size-correction through the Q-standardization proposed by Darroch and Mossiman (1985). Shape changes of functional components between deformed and undeformed skulls were evaluated on pooled samples and on each sample by means of discriminant analysis. Components that were not affected by deformation were able to be included in further comparisons. Another factor of variation among individuals within a subarea may be their ecological origin (mountains, piedmont, and plains) or localities, and even the distribution of sex with respect to localities. Since some localities provided very few individuals, it is not possible to perform statistical tests on hypotheses about differentiation among individuals according to their ecological distribution or the distribution of sex across localities. Nevertheless, the internal variation of samples of the Argentine Center-West was assessed, taking a third sample (Coimbra) as a reference. The hypothesis about the equality of variances of linear measurements was evaluated with Bartlett’s test. In this comparison, all individuals were included after a z-standardization within sexes, which is a common method to remove sex-related size variation (Williams-Blangero and Blangero, 1989; Relethford, 2001). The Coimbra sample can be considered homogenous with respect to ethnicity, geography, and temporal range. If samples of the Argentine Center-West do not differ in variances with respect to the Coimbra sample, then it is possible to deduce that such factors that may inﬂate internal variance are not important enough to affect results, and it would be justiﬁable to pool skulls together for comparisons between both subareas. Assessment of between-samples variation. Two types of indices were calculated with measurements (Pucciarelli et al., 1999; Sardi, 2002; González-José et al., 2005) (Table 3): 1) volumetric indices, represented by the geo- metric mean of three dimensions, estimate the absolute size of functional components; and 2) morphometric indices, represented by the proportion between a given volumetric index and the sum of volumetric indices that belong to the neurocranium or face, estimate the relative size of components. A paired t-test was carried out with these indices to evaluate differences between means of farmers and hunter-gatherers, and F-ratios were calculated to evaluate the equality of variances. In order to assess relative size between samples, differences between means were calculated with volumetric indices (Table 3). In order to know which dimensions intervened in the components’ differentiation, discriminant analyses with a complete estimation (i.e., including the three variables of each component) were performed on sex-pooled samples after a z-standardization within sexes. In those components that showed signiﬁcant F-values (P < 0.05), the discriminant analyses were remade with backward stepwise estimation to establish which measurements were useful for discrimination between both samples. The alpha of F-values to enter or remove variables from functions was set at 0.05. RESULTS Within-samples variation Dependence between area, sex, and deformation. Table 4 indicates that cranial deformation is a factor dependent on subarea, showing higher frequencies among farmers (Table 1), but it is uniformly distributed across the sexes. The sex factor shows a signiﬁcant dependence on subareas (Table 4), because females are more frequent among farmers (Table 1). Cranial deformation effect. Results shown in Table 5 indicate that artiﬁcial cranial deformation did not inﬂuence the shape of facial components. Skulls underwent deformation on the frontal and occipital bones. Such an effect would not affect the cranial base, which directly inﬂuences facial growth (Hilloowalla et al., 1998; Lieberman et al., 2000), not modifying facial components, but modifying the midneural and otic components (Table 5). Since deformed crania showed differences in the shape of neural components, they were excluded from the following analyses. However, they were included in analyses of facial components, because the face was not affected by deformation. Homogeneity of variances. Most variances (19/24) of samples of the Argentine Center-West and Coimbra were homeocedastic (Table 6). Heterocedastic measurements included midneural width (P < 0.05), posteroneural length (P < 0.05), posteroneural width (P < 0.01), respiratory length (P < 0.05), and masticatory width (P < 0.01). Note that Coimbra showed the greatest variances (Table 7) for most of the heterocedastic measurements. These results indicate that there was no speciﬁc factor 338 M.L. SARDI ET AL. TABLE 4. Tests of dependence between factors (subarea, sex, and deformation)1 Subarea vs. presence/absence of deformation Subarea vs. sex Sex vs. presence/absence of deformation in farmers Sex vs. presence/absence of deformation in hunter-gatherers Sex vs. presence/absence of deformation across subareas Subarea vs. sex of nondeformed skulls Subarea vs. sex of deformed skulls 1 n df v2 P-value 124 124 58 66 124 69 55 1 1 1 1 3 1 1 18.19 5.20 0.39 0.06 7.14 3.51 1.70 0.000 0.023 0.532 0.802 0.068 0.061 0.192 For comparisons with df ¼ 1, Yates-corrected v2 were calculated. TABLE 5. Effect of cranial deformation by discriminant analyses with Q-standardized variables Pooled Component Anteroneural Midneural Posteroneural Otic Optic Respiratory Masticatory Alveolar Hunter-gatherers P-value F P-value F P-value 5.82 29.08 16.85 0.55 2.21 0.55 2.46 1.36 0.001 0.000 0.000 0.646 0.089 0.644 0.065 0.259 1.47 15.69 11.36 4.71 0.18 0.49 1.46 0.49 0.230 0.000 0.000 0.005 0.910 0.688 0.232 0.685 4.23 12.01 5.99 0.61 1.25 0.67 1.40 2.65 0.009 0.000 0.001 0.608 0.298 0.570 0.253 0.057 TABLE 6. Barttlet’s test to evaluate equality of variances in samples of Argentine Center-West and Coimbra Anteroneural length Anteroneural width Anteroneural height Midneural length Midneural width Midneural height Posteroneural length Posteroneural width Posteroneural height Otic length Otic width Otic height Optic length Optic width Optic height Respiratory length Respiratory width Respiratory height Masticatory length Masticatory width Masticatory height Alveolar length Alveolar width Alveolar height Farmers F Bartlett’s v2 P-value 0.41 1.84 2.50 5.76 6.94 0.51 8.96 17.91 1.74 1.11 1.37 2.90 0.54 3.55 1.17 7.21 0.56 0.79 5.58 17.83 4.73 2.57 2.70 0.73 0.814 0.397 0.286 0.056 0.031 0.773 0.011 0.000 0.419 0.574 0.503 0.234 0.764 0.169 0.556 0.027 0.755 0.673 0.061 0.000 0.094 0.276 0.259 0.693 that inﬂated variances in samples of the Argentine Center-West, such as locality or ecological zone, enabling the samples to be compared. TABLE 7. Variances of measurements that differed between groups with Bartlett’s test Midneural width Posteroneural length Posteroneural width Respiratory length Masticatory width Hunter-gatherers Farmers Coimbra 0.69 0.53 0.57 1.07 1.07 0.57 0.25 0.25 0.57 0.64 1.09 0.74 1.08 1.03 0.48 farmers (Table 8). With respect to facial components, hunter-gatherers showed highly signiﬁcant smaller respiratory and bigger masticatory indices than farmers. The pattern of differentiation in both sexes was quite similar: females differed by the midneural, optic, and masticatory volumetric indices, and the respiratory and masticatory morphometric ones; males differed by the otic and masticatory volumetric indices, and by the anteroneural, posteroneural, and masticatory morphometric ones (Table 8). Figure 2 presents differences between means of volumetric indices, where the masticatory and posteroneural components showed the highest values. Signiﬁcant discriminant functions were calculated for the midneural, posteroneural, otic, optic, and masticatory components (Table 9). Measurements retained in the discriminant functions after backward stepwise estimations were lengths and widths, which showed higher values in hunter-gatherers than in farmers (Table 9). The otic and optic components differentiated farmers and hunter-gatherers, whereas their respective volumetric indices did not change (Table 8). Between-samples variation DISCUSSION Volumetric indices showed that hunter-gatherers’ skulls were bigger for most of the components (Table 8). When the sexes were pooled, the midneural, posteroneural, and masticatory volumetric indices were larger in hunter-gatherers. Morphometric indices varied, because hunter-gatherers presented a signiﬁcantly smaller anteroneural index, and a bigger posteroneural one than Results indicate that farmers present a smaller size for most components. The masticatory and posteroneural components show the greatest differences, with farmers presenting an absolutely and relatively smaller size than hunter-gatherers (Table 8, Fig. 2), mainly due to a reduction in length and width (Table 9). Differential gene ﬂow with populations from outside the Argentine 339 ARGENTINE CRANIOFACIAL DIFFERENTIATION TABLE 8. Paired t-test and F-ratios for comparing means and variances, respectively, of volumetric and morphometric indices (hunter-gatherers farmers) Volumetric indices Pooled sexes Anteroneural Midneural Posteroneural Otic Optic Respiratory Masticatory Alveolar Females Anteroneural Midneural Posteroneural Otic Optic Respiratory Masticatory Alveolar Males Anteroneural Midneural Posteroneural Otic Optic Respiratory Masticatory Alveolar Morphometric indices t P-value F P-value t P-value F P-value 0.25 3.08 3.95 0.54 1.60 0.55 4.99 0.71 0.804 0.003 0.000 0.585 0.111 0.578 0.000 0.480 1.00 1.39 2.47 1.01 1.04 1.39 1.45 1.24 1.000 0.437 0.034 1.000 0.861 0.204 0.149 0.407 2.53 0.46 2.78 1.87 1.91 3.05 4.51 0.88 0.013 0.647 0.007 0.065 0.057 0.002 0.000 0.380 1.58 1.61 1.55 1.18 1.78 1.42 1.07 1.21 0.275 0.256 0.297 0.712 0.027 0.173 0.777 0.442 0.80 2.76 1.90 0.71 2.30 0.84 4.56 0.89 0.430 0.009 0.067 0.480 0.025 0.405 0.000 0.374 1.46 2.07 4.28 1.03 1.04 1.65 1.99 1.04 0.510 0.203 0.014 0.977 0.944 0.189 0.074 0.890 1.13 0.74 0.89 1.84 1.63 2.74 3.58 0.57 0.266 0.462 0.381 0.076 0.107 0.008 0.000 0.567 2.54 2.28 2.61 1.33 2.32 1.17 1.23 1.31 0.106 0.149 0.096 0.617 0.029 0.674 0.576 0.511 0.53 1.72 4.24 0.03 0.15 0.00 2.87 0.15 0.600 0.093 0.000 0.973 0.877 0.999 0.005 0.877 1.58 1.27 6.79 1.10 1.05 1.20 1.02 1.47 0.371 0.595 0.023 0.767 0.923 0.632 0.975 0.311 2.73 0.13 3.59 0.84 1.15 1.73 2.98 0.68 0.009 0.891 0.000 0.406 0.255 0.087 0.004 0.494 1.25 1.02 1.98 1.12 1.42 1.66 1.10 1.17 0.844 1.000 0.398 0.742 0.363 0.186 0.767 0.638 Fig. 2. Percent differences between means (DM) of volumetric indices between hunter-gatherers and farmers. Positive values indicate greater mean value in hunter-gatherers. Center-West, stochastic mechanisms, and factors associated with the subsistence economy might explain this pattern. The fact that the Argentine Center-West samples showed low variances (Tables 6 and 7) with regard to Coimbra enables us to discard differential gene ﬂow with populations from outside the Argentine Center-West as a main factor in the increase of differentiation between hunter-gatherers and farmers. On the other hand, other factors could increase variation in Coimbra, such as less canalization, evoked by the low biomechanical demands associated with industrialization. Gene ﬂow with morphologically different populations of adjacent areas might exist in the Argentine Center-West. However, it was expected that if gene ﬂow as well as stochastic mechanisms affected morphology, then the pattern of differentiation should involve many components, without any dynamic relationship among them. In this study, the main between-samples differentiation occurred in some localized components, and it is better explained by systemic and/or localized factors associated with both subsistence economies. Greater skeletal size can be attained by the volumetric growth of functional matrices and/or by deposition of skeletal tissue (Moss et al., 1987). Among systemic factors, differences in the composition of diet and hormonal circulation would account for differentiation. Cordain (2000) estimated that most worldwide hunter-gatherer groups obtain more than 50% of their diet from animal foods, which are associated with a high percentage of energy derived from proteins, at about 19–35%. With a greater dependence on agriculture, the accessibility of animal proteins was reduced, as reported for many parts of the Andean region (Castro and Tarragó, 1992). Likewise, the higher frequency of caries in farmers than hunter-gatherers of the Argentine Center-West (Novellino and Guichón, 1997–1998) suggests an increased role of carbohydrates in the diet. Thus, a diet more deﬁcient in proteins could lead to the smaller size in farmers, as occurred in some other worldwide regions (Cohen and Armelagos, 1984). Experimental models offered insights into the effects of low-protein diets acting upon phenotypes, suggesting that these diets were associated with size reduction in many cranial and postcranial variables (Pucciarelli, 1980, 1981; Pucciarelli and Goya, 1983; Pucciarelli et al., 1990; Dressino and Pucciarelli, 1999; Miller and German, 1999; Reichling and German, 2000). However, although the protein content was lower in the farmer diet than in the hunter-gatherer diet, it is not possible to state that the farmers’ diet was so poor in proteins as were diets of those experimental models, which were under 10% of protein content. 340 M.L. SARDI ET AL. TABLE 9. Discriminant analyses performed with measurements of components Backward stepwise estimation Complete estimation F P Anteroneural Midneural Component 0.27 5.37 0.844 0.002 Posteroneural Otic 7.43 3.39 0.000 0.023 11.08 2.15 12.04 0.000 0.097 0.000 1.01 0.388 Optic Respiratory Masticatory Alveolar Variables retained with alpha ¼ 0.05 Length, F ¼ 8.07 Width, F ¼ 7.74 Width, F ¼ 16.26 Length, F ¼ 5.24 Width, F ¼ 6.33 Length, F ¼ 29.14 Length, F ¼ 12.66 Width, F ¼ 6.64 Hormonal action may be linked to differences in mobility. Weltman et al. (2001) found a direct association between growth hormone circulation and physical activity. In humans, the circulation of growth hormones was recorded from birth (Geary et al., 2003). Growth hormone promotes the increment in skeletal (Vogl et al., 1993; Barr and McKay, 1998; Banu et al., 2001; Forwood et al., 2001) and muscle mass (Vogl et al., 1993), and it inﬂuences craniofacial growth (Oyhenart and Pucciarelli, 1992; Cónsole et al., 2001). The settlement pattern in the northern subarea, the greater concentration of archaeological material, and the use of animals for transport revealed that farmers were less mobile than hunter-gatherers. But if the reduced circulation of growth hormone led to a size reduction in farmers, then farmers should present greater reduction in the face than in the neural skull, because facial structures are under greater hormonal inﬂuence. Moreover, the neural skull grows at high rates at early infancy, and differences in mobility between hunter-gatherers and farmers during this ontogenetic period seem unlikely. However, hormonal inﬂuence in a certain proportion of facial variation, at least, cannot be completely excluded. Hormonal factors might interact with nutritional factors, since the mechanisms that regulate growthhormone secretion are sensitive to nutritional status. In this sense, Cónsole et al. (2001) found that a low-protein diet in monkeys induced a decrease in growth hormone and prolactin cell populations, resulting in changes of craniofacial morphology. Among localized factors, mechanical loading acting upon the masticatory complex and neck due to differences in food consistency between hunter-gatherers and farmers could promote differentiation. The bigger masticatory size of hunter-gatherers may be the result of greater masticatory stress, which was reduced in farmers. Masticatory forces regulate an important proportion of craniofacial growth, affecting several structures (e.g., Hannam and Wood, 1989; van Spronsen et al., 1991; Kiliaridis, 1995). According to Raadsheer et al. (1999), the magnitude of masticatory forces is positively correlated with muscular thickness and facial measurements. Kiliaridis (1995) proposed that masticatory hyperfunction led to facial size enlargement through sutural growth and bone apposition. Experimental studies suggest that the mastication of soft diets contributes to many changes, such as a reduction in cortical bone thickness (Bresin et al., 1999), shortening of maxillary arches and deformation of the palate (Beecher et al., 1983), reduction of muscular size (Ciochon et al., 1997), modiﬁcations Mean of scores obtained with discriminant function Farmers Hunter-gatherers 0.73 0.30 0.76 0.61 0.31 0.25 0.51 0.45 0.57 0.50 of the mandibular condile (Giesen et al., 2003), and lesser growth, particularly in transverse dimensions and in posterior portions of the skull (Lieberman et al., 2004). Signiﬁcant modiﬁcations located in the masticatory component were reported. Analyses of minipigs showed that the masseter pulls on the zygomatic bone during mastication, and great mechanical loadings are produced in the zygomatico-squamosal suture and bone surfaces (Rafferty et al., 2000; Herring et al., 2001). In hyraxes, the highest strains generated by processing hard food are located mainly in the zygomatic arch (Lieberman et al., 2004). Comparative studies in temporal scales (Carlson and Van Gerven, 1979; Varrela, 1992; Kaifu, 1997; Sardi et al., 2004) are quite consistent with experimental models and with the ﬁndings of this study. Carlson and Van Gerven (1979) compared Mesolithic and later groups of Lower Nubia, and found that later groups presented a reduction in size of the masticatory muscles and teeth, a reduction in facial growth, changes in facial position, and a cranial vault with a relatively shorter and higher shape. Sardi et al. (2004) compared samples of Europe and North Africa, and observed that post-Mesolithic groups were characterized by smaller size, narrower faces, and more reduced masticatory volume than Paleolithic and Mesolithic huntergatherers. It is possible that the shift observed in both studies (Carlson and Van Gerven, 1979; Sardi et al., 2004) was due to farmer demic diffusion and population replacement (Ammerman and Cavalli-Sforza, 1984; Turner and Markowitz, 1990). However, the fact that differentiation is located in speciﬁc structures supports the proposal that diet-related factors account for at least part of the craniofacial variation. Other studies (Smith, 1979; Lahr and Arensburg, 1995) proposed that a decrease of workload on the face during the Neolithic transition was associated with a tendency toward brachycephalization. Masticatory forces can also explain the posteroneural differentiation. Herring and Teng (2000) and Herring et al. (2001) analyzed minipigs, and demonstrated that the contraction of the masseter and temporalis during natural mastication caused strains in some sutures of the braincase. Since minipigs move their heads during mastication, the neck muscles were also affected (Herring and Teng, 2000). In humans, a similar high degree of coordination between concomitant mandibular and head-neck movements during natural jaw activities was reported (Zafar et al., 2000). This functional relationship apparently relies on common neural connections that control activities in both systems (Igarashi et al., 2000; ARGENTINE CRANIOFACIAL DIFFERENTIATION Zafar et al., 2000). Thus, the bigger postneural size in hunter-gatherers may reﬂect the greater masticatory activity on neck muscles, which are attached to the occipital bone. CONCLUSIONS The above results support the hypothesis that craniofacial differentiation between farmers and hunter-gatherers of the Argentine Center-West was affected by dietrelated factors. Farmers presented a smaller craniofacial size, and showed absolute and relative reductions of the masticatory and posteroneural components with respect to hunter-gatherers. Two systemic factors, 1) the lower quality of nutrition due to low protein content in the diet, and 2) the diminution of growth hormone circulation because of lesser mobility due to sedentism, and a localized factor, the reduction of masticatory stress and workload on the head and neck, could generate this pattern. Although nutritional and hormonal factors can account for a certain proportion of craniofacial size variation, the pattern of differentiation seems to suggest localized rather than systemic factors. The size reduction of the masticatory and posteroneural components in farmers can be attributed to lesser muscular loadings due to the softer consistency of the diet consumed after the transition to food production. ACKNOWLEDGMENTS We thank our reviewers for their contributions to the improvement of the manuscript; Rolando González-José and Fernando Ramı́rez Rozzi, for useful commentaries that helped clarify some aspects of our argument; Vı́ctor Durán, Humberto Lagiglia, Gabriela Raviña, and Marta Roa, for assistance in archaeological aspects; Pablo Sardi, Rodrigo Lacruz, and Marı́a C. Muñe, for technical assistance; and the curators of the collections for access to specimens in their care. This work was made possible by grants from the Universidad Nacional de La Plata (Argentina) and the Fondation Fyssen (France) to M.L.S. LITERATURE CITED Albanese J. 2003. A metric method for sex determination using the hipbone and the femur. J Forensic Sci 48:263–273. Ammerman AJ, Cavalli-Sforza LL. 1984. The Neolithic transition and the genetics of population in Europe. Princeton: Princeton University Press. Anton SC. 1989. 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