Common features of sexual dimorphism in the cranial airways of different human populations.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 146:414–422 (2011) Common Features of Sexual Dimorphism in the Cranial Airways of Different Human Populations Markus Bastir,1* Paula Godoy,2 and Antonio Rosas1 1 Paleoanthropology Group, Department of Paleobiology, Museo Nacional de Ciencias Naturales, CSIC; Calle J. G Abascal 2, 28006, Madrid, Spain 2 Facultad de Ciencias, Autónoma University Madrid, Cantoblanco, Crtra. Colmenar Viejo 34, 28049, Madrid KEY WORDS morphometrics human craniofacial variation; cranial airways; respiratory apparatus; geometric ABSTRACT Sexual dimorphism in the human craniofacial system is an important feature of intraspeciﬁc variation in recent and fossil humans. Although several studies have reported different morphological patterns of sexual dimorphism in different populations, this study searches for common morphological aspects related to functional anatomy of the respiratory apparatus. 3D geometric morphometrics were used to test the hypothesis that due to higher daily energy expenditure and associated greater respiratory air consumption as well as differences in body composition, males should have absolutely and relatively greater air passages in the bony cranial airways than females. We measured 25 3D landmarks in ﬁve populations (N 5 212) of adult humans from different geographic regions. Male average cranial airways were larger in centroid sizes than female ones. Males tended to show relatively taller piriform apertures and, more consistently, relatively taller internal nasal cavities and choanae than females. Multivariate regressions and residual analysis further indicated that after standardizing to the same size, males still show relatively larger airway passages than females. Because the dimensions of the choanae are limiting factors for air transmission towards the noncranial part of the respiratory system, the identiﬁed sex-speciﬁc differences in cranial airways, possibly shared among human populations, may be linked with sex-speciﬁc differences in body size, composition, and energetics. These ﬁndings may be important to understanding trends in hominin facial evolution. Am J Phys Anthropol 146:414–422, 2011. V 2011 Wiley-Liss, Inc. Sexual dimorphism is an important source of intraspeciﬁc craniofacial variation in recent and fossil humans (Acsádi and Nemeskéri, 1970; Wood, 1976; Smith, 1980; Frayer and Wolpoff, 1985; Plavcan and Schaik, 1994; Rehg and Leigh, 1999; Rosas and Bastir, 2002; Rosas et al., 2002; Bastir et al., 2006; Bulygina et al., 2006; Bastir, 2008; Bastir et al., 2010b). It has been suggested that different populations and species express sexual dimorphism in different patterns and magnitudes, depending on variation among proximate and ultimate factors such as sexual selection, mating patterns, variation in body size, economic patterns and non-economic role patterns (Frayer and Wolpoff, 1985, Kaplan et al., 2000; Puts, 2010). However, despite such population differences in craniofacial sexual dimorphism there is also reason to hypothesize common features, related to metabolic and energetic factors. In particular, respiratory physiology in relation to the energy household of the organism may be an important factor of craniofacial variation (Bastir, 2008). Respiratory function is crucially involved in the total energy budget in animals via basal metabolism and activity patterns and thus daily energetic expenditure (DEE) (Leonard and Ulijaszek, 2002). Although absolute DEE values vary depending on climatic background of the analyzed populations and the estimation methods (Steegmann et al., 2002; Churchill, 2006; Froehle and Churchill, 2009) recent estimates in H. sapiens suggest that, on average, the daily energy expenditure in males is 30% higher than in females (Froehle and Churchill, 2009). Such physiological differences are caused by sexspeciﬁc differences in body mass, but also body composition (percentage of lean muscle mass), and are reﬂected at a morpho-functional level by differences in oxygen consumption and pulmonary capacity (Silbernagl and Despopoulos, 1991; Bitar et al., 2000; Siervogel et al., 2003; Hall, 2005; Wells, 2007). Data presented by Hall (2005) showed links between daily energy expenditure and oxygen consumption with respect to cranial airways. She showed that the volume of consumed oxygen via mouth breathing differed signiﬁcantly among sexes (294 ml/min in males and 243 ml/ min in females), and also, that sex-speciﬁc differences in nose breathing subjects were statistically even clearer (males: 250 ml/min; females: 203 ml/min; [Hall, 2005]). On a less empirical basis, Enlow (1968, 1990) related sex-speciﬁc differences in strength and muscularity causally to sexual dimorphism in airway and thus craniofacial morphology. This has been conﬁrmed, by two-dimensional geometric morphometric analysis of craniofacial sexual dimorphism, which indicated that males differed in size and shape in a way that allowed processing C 2011 V WILEY-LISS, INC. C Grant sponsor: SYNTESYS SYS-resources. Grant sponsor: MEC, Spanish Ministry of Education and Science; Grant numbers: CGL2009-09013. *Correspondence to: Markus Bastir, Paleoanthropology Group, Museo Nacional de Ciencias Naturales, CSIC, Calle J. G Abascal 2, 28006; Madrid, Spain. E-mail: email@example.com Received 29 December 2010; accepted 7 July 2011 DOI 10.1002/ajpa.21596 Published online 24 August 2011 in Wiley Online Library (wileyonlinelibrary.com). FUNCTIONAL NASOPHARYNX MORPHOLOGY TABLE 1. Landmarks Count 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Label Nasion Rhinion Anterior nasal spine Right optic canal point Right foramen ethmoidalis posterius Right foramen ethmoidalis anterius Right dacryon Right distal naso-maxillary junction Right lateral piriform point Left optic canal point Left foramen ethmoidalis posterius Left foramen ethmoidalis anterius Left dacryon Left distal naso-maxillary junction Left lateral piriform point Hormion Staphylion Pharyngeal tubercle Basion Right lateral palatine angle Right posterior inferior turbinate insertion Right choana base Left lateral palatine angle Left posterior inferior turbinate insertion Left choana base larger respiratory air volumes than females (Rosas and Bastir, 2002). In that study we partitioned sexual dimorphism in two components: an allometric component, related to overall skull proportions and a nonallometric component, related to speciﬁc modiﬁcations of the nasopharyngeal skeleton and other, musculo-skeletal features, more localized at the skull. Thus, it has been speculated that differences in absolute and relative airway proportions might relate to sex-differences in body size (absolute airway size) and body composition (relative airway size) (Rosas and Bastir, 2002). Longitudinal ontogenetic analyses of other populations have shown that males develop both absolutely and relatively larger midfacial dimensions than females possibly indicating greater airway passages (Bastir et al., 2006; Bulygina et al., 2006). Differences in male and female nasal volumes have been discussed with respect to energetics of nose and mouth-breathing (Hall, 2005). Also, one preliminary geometric morphometric study of nasal endocasts has indicated signiﬁcant differences in absolute and relative dimensions of the nasal cavity, particularly highlighting sexual dimorphism at the choanae (Garcia-Tabernero, 2005; Bastir et al., 2009). These observations might provide evidence for a direct morpho-functional relationship between human skull variation and physiological factors of the musculoskeletal and metabolic system of the organism (Bastir, 2008). In particular, such relations could be involved in systemic and thus nonrandom trends in facial evolution in Homo (Rosas and Bermudez de Castro, 1998; Trinkaus, 2003; Bastir, 2008; Yokley et al., 2009; Bastir and Rosas, 2011). However, morpho-functional interpretations of skeletal morphology of recent or fossil humans would greatly beneﬁt from extending this focus to other populations and larger data sets. Also, interpretations derived from 2D data might differ from a proper 3D analysis of the skeletal cranial airways. The aim of this study is therefore to analyze the 3D conﬁguration of the human 415 nasopharynx in different human populations and to test the hypothesis that males have absolutely and relatively larger airways than females. MATERIALS AND METHODS This study uses geometric morphometrics to analyze size, shape, and form (i.e., size plus shape) of 3D conﬁgurations of 25 landmarks (Table 1) measured on the skeletal cranial airways of 212 adult specimens of different geographic populations: Coimbra, housed at the University of Coimbra, Portugal, (N 5 72), (Rocha, 1995), the Spitalﬁelds collection in London, UK (N 5 77) (Molleson et al., 1993; Middleton and Rassam, 1995), the African Ibo-tribe (N 5 34) (Middleton and Rassam, 1995), and two smaller samples from Australia (N 5 17) and NorthAmerica (Inuit) sample (N 5 11), housed at the Natural History Museum London and the University of Cambridge. Details of the collections and data recording process have been described elsewhere (Rosas and Bastir, 2002; Bastir and Rosas, 2004; Bastir et al., 2004). Sex was known for Coimbra and Spitalﬁelds and assessed on standard anthropological criteria on the remaining populations. We cross-checked our sex-assessment further with assessments used in other studies by other authors (Strand-Viðarsdóttir et al., 2002; Franklin et al., 2007). Except for one case in the Australian population there was an identical sex assessment. Thus, the case in question was removed from the sample. Missing data were few and estimated using a multiple multivariate regression model based on the full data set (Slice, 2000; Bastir et al., 2008; Gunz et al., 2009; Neeser et al., 2009). Centroid size (CS) was analyzed by ANOVAs and t-tests. Mean shape differences were tested by permutation analyses (N 5 10.000) of Procrustes distances and Mahalanobis distances. Shape data were made symmetric by reﬂected relabeling (Mardia et al., 2000) prior to analysis using MorphoJ software (Klingenberg, 2008– 2010). Male and female mean shapes were then compared for each population as well as of a pooled population sample. Allometry, and differences of slopes among sexes were analyzed ﬁrst by MANCOVA (PC-scores, CS, sex) and then by multivariate regression of Procrustes shape coordinates on centroid size in the full data set of the pooled within-sex variance (111 females, 101 males). Male and female means of the non-allometric residuals were compared. Finally, we rescaled the overall male and female mean shapes with male and female mean centroid sizes to visualize sexual dimorphism in form space. All results were visualized using MorphoJ software and the Morpheus Visualization tool (Slice, 1998). ANOVAs, MANOVAs and MANCOVAs were performed in Statistica 6.0 (StatSoft, 1999). RESULTS In all populations males were signiﬁcantly larger than females while no size differences were found between the populations (Table 2, Fig. 1). Also, in the pooled populations the centroid sizes were signiﬁcantly different: females (N 5 111): CS 5 165.9; males (N 5 101): CS 5 176.1; t 5 212.65; df 5 210; P \ 0.0001 as were the variances (female std. dev. 5 5.1; male std. dev. 5 6.5; Fratio 5 1.6; P \ 0.02). American Journal of Physical Anthropology 416 M. BASTIR ET AL. Mean shapes differences are shown in Table 3 and Figures 2 and 3. Procrustes distances were signiﬁcantly different for the larger samples of Coimbra, Spitalﬁelds, marginally different in the Australian sample and not signiﬁcant in the African and Inuit samples. Mahalanobis distances were signiﬁcantly different in all populations except Australians. The mean shape of all males was signiﬁcantly different from the mean shape of all females. Morphologically, mean shape differences showed common as well as different features. The most striking feature was the increased absolute and relative height of the male choanae in all populations compared to the reduced height in females (see Fig. 2). Figures 2 and 3 TABLE 2. Centroid size differences, ANOVA (centroid size, sex and populations) Population Sex population*sex Error SS Degr. of MS F P 116 3179 196 6860 4 1 4 202 29 3179 49 34 0.9 93.6 1.4 0.495 0.000 0.222 also show that each population displays some unique features of sexual dimorphism. Coimbra, Spitalﬁelds, (see Fig. 2), Australians and Inuit (see Fig. 3) vary in the external spheno-occipital clivus orientation, while the African sample (Fig. 2c) shows much less variation in this respect. Coimbra males (Fig. 2a) also have relatively taller piriform apertures and are similar to the Ibo-tribe (Fig. 2c) and Australians (Fig. 3a) in this feature contrary to the Spitalﬁelds (Fig. 1b) and Inuit (Fig. 3b) males. These differences of relative anterior and posterior nasal cavity heights in sexual dimorphism are also reﬂected in the relative orientation of the nasal ﬂoor. Coimbra, Spitalﬁelds, and Ibo males (see Fig. 2) show increased relative cavity heights in the centre of the nasal cavity, a feature that is not so clear in the Australian and Inuit populations (see Fig. 3). When pooled together (Fig. 3c), these subtleties disappear and mainly the vertical differences remain. The overall patterns of shape dimorphism did not differ statistically among the populations (Table 4). MANCOVA revealed that allometry was highly signiﬁcant and also signiﬁcantly different among males and females (Table 5). Pooled within-group allometry was Fig. 1. Mean comparisons of male and female centroid sizes among populations. In each population males are consistently and signiﬁcantly larger than females. Ranges vary according to sample sizes. American Journal of Physical Anthropology FUNCTIONAL NASOPHARYNX MORPHOLOGY statistically signiﬁcant (P 5 0.0007) and accounted for 2% of variation. Figure 4a shows the allometric variation pattern and Figure 4b the nonallometric shape differences between males and females, which indicate that the anterior nasal opening in males is relatively taller, and slightly narrower. Also, the choanae and the internal nasal cavity are relatively taller in males compared to females and no medio-lateral variation is observed. Form space comparisons (mean shapes rescaled by mean centroid sizes) in Figure 5 show how absolute and relative vertical dimensions differ at the choanae, in the middle of the nasal cavity and at the piriform aperture TABLE 3. Mean shape comparisons; d 5 Procrustes distance, Md 5 Mahalanobis distance (P-value assessed by 10,000 permutations of group membership) Coimbra Spitalﬁelds IBO AUS INU Total d P-value Md P-value 0.02 0.02 0.02 0.05 0.05 0.02 0.04 0.003 0.3 0.09 0.2 0.0002 2.1 2.83 6.8 1.9 2.26 1.57 \0.0001 \0.0001 \0.0001 0.3 0.04 \0.0001 417 (Fig. 5a,b). Also the epipharynx is relatively increased due to vertical and antero-posterior enlargement. The upper anterior nasal part projects more in males than in females (Fig. 5a). In top view, males and females do not differ in their inter-orbital breadths at the upper nasal cavity (Fig. 5c) while males show a higher nasal saddle (Fig. 5a) and a slightly narrower piriform aperture (Fig 5c,d). DISCUSSION This study aimed to compare patterns of sexual dimorphism in the human nasopharyngeal skeleton among different populations. Our ﬁndings support previous hypotheses of a common structural factor inherent in human skull dimorphism which implies relatively (Rosas and Bastir, 2002) and absolutely (Enlow, 1990; Rosas and Bastir, 2002) larger airways in males than in females. Centroid size differences between males and females were slightly smaller in Coimbra than in Spitalﬁelds (see Fig. 1). African IBO sample and the Inuit populations showed greater male–female size differences. It is known that magnitudes and patterns of sexual Fig. 2. Mean shapes of males (dashed, black) and females (solid, gray) (33 magniﬁed). (a) Coimbra (the numbers correspond to landmark counts given in Table 1), (b) Spitalﬁelds, (c) Ibo-tribe. Note that in all populations the relative vertical height at the choanae is increased in males compared with females while other features are more variable. American Journal of Physical Anthropology 418 M. BASTIR ET AL. Fig. 3. Mean shapes of males (dashed, black) and females (solid, gray) (33 magniﬁed). (a) Australians, (b) Inuit, (c) all populations. Note that in all populations the relative vertical height at the choanae is increased in males compared with females while other features are more variable. dimorphism vary among populations (for example, Rosas et al., 2002) and the results on size differences from Coimbra and Spitalﬁelds ﬁt with these observations. Nevertheless, differences observed in populations, in which sex was unknown and was thus assessed by skeletal criteria, could also reﬂect bias due to the sexing procedure. Both analyses of individual populations, as well as of the pooled sample in shape and form space indicated consistently vertically taller choanae in males than females. This is particularly interesting because the anterior opening of the airways did not differ that consistently between males and females among different populations. This suggests different patterns of sexual dimorphism in anterior facial regions (including piriform aperture) that relate possibly to differences in the population structure and genetic history of these groups or other factors (Frayer and Wolpoff, 1985). Greater population variability at anterior cranial airways contrasts with lower and common variability features at the posterior cranial airways (absolute and relative choanae height). It ﬁts with physiological differences of respiratory physiology because larger choanae in males permit inhalation of greater air volume to enter the non-cranial American Journal of Physical Anthropology respiratory system than smaller female choanae (Mlynski et al., 2001). Recent somatometric studies have shown that males differed from females in nose volume (Hall, 2005). This corresponds well to the signiﬁcant size differences found here (see Fig. 1). However, Hall (2005) suggested sexual dimorphism of nasal height, width and length, but not projection. Our data indicate that at a skeletal level the upper nasal skeleton projects more forwards beyond the nasal ﬂoor in males than in females. Hall (2005) associated morphological differences observed in her study with an energetic background. Due to differences in body mass, males have a higher daily energy expenditure than females (Steegmann et al., 2002; Churchill, 2006; Froehle and Churchill, 2009). This is linked to approximately 20% greater oxygen consumption (Hall, 2005), which is further reﬂected by absolute and relative differences in lung capacity (Silbernagl and Despopoulos, 1991). However, magnitudes of sex-differences in energy expenditure, oxygen consumption and cranial airway size are not proportional: When male mean values are set 100%, average daily energy expenditure in females of different climatic origin is about 71% (male mean: 3569 kcal, female mean: 2544 kcal; Steegman et al., 2002; Froehle and Churchill, 2009), female oxygen consumption 419 FUNCTIONAL NASOPHARYNX MORPHOLOGY is about 81% (male mean: 250 ml, female mean: 203 ml) (Bitar et al., 2000; Hall, 2005) and female cranial airway sizes approach 94% of male mean size (male mean centroid size 176.1; female mean centroid size: 165.9; Fig. 1). Further study should address the functional background of these different proportions. Sex-speciﬁc differences in the nasal region can also be inferred from the study of Bulygina et al. (2006). These authors performed a 2D geometric morphometric study of sexual dimorphism ontogeny, although they did not measure explicitly nasal and midfacial anatomy. However, Figure 7 in their paper seems to indicate that adult males differed from females—among other features—by a forward projection of the upper nasal area and an overall expansion of the midface, a difference that these authors described as increased facial prognathism (Bulygina et al., 2006). It would be interesting to determine when during growth this kind of differences start to arise. Two-dimensional analysis of ontogenetic longitudinal x-ray data did show consistently larger airways in males compared to females at all ontogenetic stages (Bastir et al., 2009), but differences in shape could not be identiﬁed doubtlessly for given ages due to low quality of the x-ray images (Bastir et al., 2006; Bulygina et al., 2006). Assuming the morpho-functional links between midfacial shape and respiratory physiology hypothesized here, nasal cavity shape differences should not occur later than puberty, when sex-speciﬁc differences in body composition (fat mass, fat free [muscle] mass) have been detected (Bitar et al., 2000; Siervogel et al., 2003; Wells, 2007). While the energy expenditure of prepubertal boys (ca. 1851 kcal/d) is higher than that of girls (ca. 1715 kcal/d) around puberty these differences become more acute (pubertal boys: ca. 3294 kcal/d, pubertal girls: ca. 2807 kcal/d) due to changes in body composition and internal muscle tissue metabolic activity (Bitar et al., 2000). Sexspeciﬁc energetic differences in these ontogenetic ages are also accompanied by differences in the consumption of respiratory air (peak VO2) (Bitar et al., 2000). A straightforward translation of these physiological observations into a skeletal maturation analysis would lead to the following expectation: before puberty sexdifferences between boys and girls would be mainly due to ontogenetic scaling (reﬂecting differences in body size). Afterwards and in adults (as shown in this study) both allometric and nonallometric skeletal differences in airway-proportions should be expected (reﬂecting differences in body size and body composition). If supported, it would lend further strength to energetic interpretations of skeletal airway conﬁguration and its possible interaction with craniofacial morphology, important to human facial evolution (Trinkaus, 2003; Bastir, 2004; Rosas et al., 2006; Bastir, 2008; Yokley et al., 2009; Bastir et al., 2010a) and evolutionary energetics (Leonard and Ulijaszek, 2002; Churchill, 2006; Yokley et al., 2009). The large bodies of Middle Pleistocene TABLE 4. MANOVA (PC-scores, sex, populations) TABLE 5. MANCOVA (PC-scores, centroid size, sex) Test Intercept Population Sex Population*sex Wilks Wilks Wilks Wilks Value L L L L 0.520275 0.01572 0.632153 0.412359 F Effect Error 4.136816 37 166 8.237703 148 663.9775 2.610663 37 166 1.117268 148 663.9775 P 0.000 0.000 0.000 0.184 Test Intercept Sex CS Sex*CS Wilks Wilks Wilks Wilks L L L L Value F Effect Error P 0.671354 0.75641 0.669745 0.755496 2.275644 1.497023 2.29227 1.504459 37 37 37 37 172 172 172 172 0.000 0.045 0.000 0.043 Fig. 4. Allometry and residual analysis (magniﬁed). (a) allometric variation: dashed, black lines show shapes associated to larger centroid size; solid, gray lines show shapes associated to smaller centroid size); (b) non-allometric shape differences between males (dashed, black) and females (solid, gray). American Journal of Physical Anthropology 420 M. BASTIR ET AL. Fig. 5. Male and female landmark conﬁgurations in form space (size and shape). Males: black outlines connecting the squares; females: gray outlines connecting the spheres. (a) lateral view; (b) frontal view; (c) top view, (d) 3D aspect from a left anterior, superior point of view. humans from Africa and Eurasia (Ruff, 2010), assumably characterized by an enormous daily energy expenditure (Churchill, 2006), were likely an important factor in the evolution of some aspects of skull proportions in these large-faced human species (Rosas and Bermudez de Castro, 1998; Trinkaus, 2003; Rosas et al., 2006; Bastir, 2008; Yokley at al., 2009; Bastir et al., 2010a, Bastir and Rosas, 2011). In this context several important questions need to be addressed: How do anterior and posterior nasal structures interact with each other and with the face? Knock-on effects of nasal cavity morphology on facial form are being discussed controversially (Chierci et al., 1973; Rosas and Bastir, 2002). Experimental and other data suggest certain independence between the nasal capsule and the surrounding face (Chierci et al., 1973; Anton, 1989; Franciscus, 2003), while on the other hand, the fact that males and females do not only differ in absolute and relative facial size (Rosas and Bastir, 2002; Strand-Viðarsdóttir et al., 2002; Bastir et al., 2006; Bulygina et al., 2006) but also in absolute and relative nasopharynx size may suggest the contrary. Preliminary results on facial and nasal cavity integration studies provide evidence for moderate morphological integration (Bastir and Rosas, 2011). Importantly related to these issues is the relationship of internal and external nasal morphology and its bearing for respiratory performance, i.e. conditioning, moistening and gas-exchange (Dean, 1988; Franciscus and Long, 1991; Mlynski et al., 2001; Churchill et al., 2004; Yokley, 2009). Modularity can be expected because different regions are apparently responsible for different functional tasks (Mlynski et al., 2001; Yokley, 2009). American Journal of Physical Anthropology However, while more ontogenetic and experimental data are necessary for a rigorous testing of evolutionary hypotheses, currently there is growing evidence to indicate that respiratory function and energy expenditure may play an important role in sexual dimorphism of the skeletal morphology in the modern human midface. ACKNOWLEDGMENTS The authors are grateful to Eugenia Cunha (University of Coimbra, Portugal), Louise Humphrey, Chris Stringer, and Robert Kruszynski at the NHM-London (UK) and to Marta Mirazon, Robert Foley and Maggie Belattie (Leverhulme Centre for Human Evolutionary Studies, University of Cambridge, UK) for assistance and hosting during the time of data acquisition. Una Strand-Vidasdottir and Dan Franklin kindly shared their sex-assessments on African and Australian skull collections. Paul O’Higgins and Robert Franciscus provided helpful comments on discussions on these and related issues. LITERATURE CITED Acsádi G, Nemeskéri J. 1970. History of human life span and mortality. Budapest: Akadémiai Kiadó. Anton SC. 1989. Intentional cranial vault deformation and induced changes of the cranial base and face. Am J Phys Anthropol 79:253–267. Bastir M. 2004. A geometric morphometric analysis of integrative morphology and variation in human skulls with implications for the Atapuerca-SH hominids and the evolution of FUNCTIONAL NASOPHARYNX MORPHOLOGY Neandertals. Structural and systemic factors of morphology in the hominid craniofacial system [Doctoral Dissertation]. Madrid: Autonoma University of Madrid. Bastir M. 2008. A systems-model for the morphological analysis of integration and modularity in human craniofacial evolution. J Anthropol Sci 86:37–58. Bastir M, Garcı́a Tabernero A, Rosas A. 2009. Geometric morphometrics of the human nasal cavity. Paleontologia i evolució 3:25–26. Bastir M, Rosas A. 2004. Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. J Hum Evol 47:359–381. Bastir M, Rosas A. 2011. Nasal form and function in Mid-Pleistocene human facial evolution. A ﬁrst approach. Am J Phys Anthropol 144:83. Bastir M, Rosas A, Kuroe K. 2004. Petrosal orientation and mandibular ramus breadth: evidence of a developmental integrated petroso-mandibular unit. Am J Phys Anthropol 123:340–350. Bastir M, Rosas A, Lieberman DE, O’Higgins P. 2008. Middle cranial fossa anatomy and the origins of modern humans. Anat Rec 291:130–140. Bastir M, Rosas A, O’Higgins P. 2006. Craniofacial levels and the morphological maturation of the human skull. J Anat 209:637–654. Bastir M, Rosas A, Stringer C, Cuétara Pastor JM, Kruszynski R, Weber GW, Ross CF, Ravosa MJ. 2010a. Effects of brain and face size on basicranial form in human and primate evolution. J Hum Evol 58:424–431. Bastir M, Rosas A, Tabernero AG, Peña-Melián A, Estalrrich A, de la Rasilla M, Fortea J. 2010b. Comparative morphology and morphometric assessment of the Neandertal occipital remains from the El Sidrón site (Asturias. Spain: years 2000– 2008). J Hum Evol 58:68–78. Bitar A, J.Vernet, Coudert J, Vermorel M. 2000. Longitudinal changes in body composition, physical capacities and energy expenditure in boys and girls during the onset of puberty. Eur J Nut 39:157–163. Bulygina E, Mitteroecker P, Aiello L. 2006. Ontogeny of facial dimorphism and patterns of individual development within one human population. Am J Phys Anthropol 131:432–443. Chierci G, Harvold EP, Vagervik K. 1973. Morphogenetic experiments in facial asymmetry: the nasal cavity. Am J Phys Anthropol 38:291–300. Churchill SE. 2006. Bioenergetic perspectives on Neanderthal thermoregulatory and activity budgets. In: Harvati K, and Harrison T, editors. Neanderthals revisited. New York City: Springer Verlag. p113–156. Churchill SE, Shackelford LL, Georgi JN, Black MT. 2004. Morphological variation and airﬂow dynamics in the human nose. Am J Hum Biol 16:625–638. Dean M. 1988. Another look at the nose and the functional signiﬁcance of the face and nasal mucous membrane for cooling the brain in fossil hominids. J Hum Evol 17:715–718. Enlow DH. 1968. The human face: an account of the postnatal growth and development of the craniofacial skeleton. New York: Harper & Row. Enlow DH. 1990. Facial growth. Philadelphia: W. B. Saunders Company. Franciscus RG. 2003. Comparing internal nasal fossa dimensions and classical measures of the external nasal skeleton in recent humans: inferences for respiratory airﬂow dynamics and climatic adaptation. Am J Phys Anthropol S 36:96–97. Franciscus RG, Long JC. 1991. Variation in human nasal height and breadth. Am J Phys Anthropol 85:419–427. Franklin D, Freedman L, Milne N, Oxnard CE. 2007. Geometric morphometric study of population variation in indigenous southern African crania. Am J Hum Biol 19:20–33. Frayer D, Wolpoff M. 1985. Sexual dimorphism. Annu Rev Anthropol 14:429–473. Froehle A, Churchill SE. 2009. Energetic competition between Neandertals and anatomically modern humans Paleoanthropol 2009:96–116. 421 Garcia-Tabernero A. 2005. Estimacion de los volumenes craneales internos en homı́nidos mediante tecnicas de antropologı́a virtual: cavidad nasal [Master Thesis]. Madrid: University Complutense. Gunz P, Mitteroecker P, Neubauer S, Weber GW, Bookstein FL. 2009. Principles for the virtual reconstruction of hominin crania. J Hum Evol 57:48–62. Hall RL. 2005. Energetics of nose and mouth breathing, body size, body composition, and nose volume in young adult males and females. Am J Hum Biol 17:321–330. Kaplan H, Hill K, Lancaster J, Hurtado AM. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185. Klingenberg CP. 2008–2010. MorphoJ. Manchester: University of Manchester. Leonard W, Ulijaszek S. 2002. Energetics and evolution: an emerging research domain. Am J Hum Biol 14:547–550. Mardia KV, Bookstein FL, Moreton IJ. 2000. Statistical assessment of bilateral symmetry of shapes. Biometrika 87: 285–300. Middleton J, Rassam A. 1995. Ibo. Encyclopedia of world cultures. Boston: G. K. Hall and Co. p120–124. Mlynski G, Grützenmacher S, Plontke S, Mlynski B. 2001. Correlation of nasal morphology and respiratory function. Rhinology 39:197–201. Molleson T, Cox M, Waldron A, Whittaker DK. 1993. The named sample. In: Molleson T, Cox M, Waldron A, and Whittaker DK, editors. The Spitalﬁelds Project Volume 2: The anthropology: The middling sort, CBA Research Report 86. York: Council for British Archaeology. p 93–122;157–166. Neeser R, Ackermann RR, Gain J. 2009. Comparing the accuracy and precision of three techniques used for estimating missing landmarks when reconstructing fossil hominin crania. Am J Phys Anthropol 140:1–18. Plavcan JM, Schaik CPV. 1994. Canine dimorphism. Evol Anthropol 2:208–214. Puts DA. 2010. Beauty and the beast: mechanisms of sexual selection in humans. Evol Hum Behav 31:157–175. Rehg JA, Leigh SR. 1999. Estimating sexual dimorphism and size differences in the fossil record: a test of methods. Am J Phys Anthropol 110:95–104. Rocha MA. 1995. Les collections ostéologiques humaines identiﬁées du Musee Anthropologique de l’Université de Coimbra. Antropologia Portuguesa 13:7–39. Rosas A, Bastir M. 2002. Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex. Am J Phys Anthropol 117:236–245. Rosas A, Bastir M, Martı́nez Maza C, Bermúdez de Castro JM. 2002. Sexual dimorphism in the Atapuerca-SH hominids. The evidence from the mandibles. J Hum Evol 42:451–474. Rosas A, Bermudez de Castro JM. 1998. The Mauer mandible and the evolutionary signiﬁcance of Homo heidelbergensis. Geobios 31:687–697. Rosas A, M.Bastir, C.Martı́nez-Maza, Garcı́a-Tabernero A, Lalueza-Fox C. 2006. Inquiries into Neanderthal cranio-facial development and evolution: ‘accretion’ vs. ‘organismic’ models. In: Harrison T, Harvati K, editors. Neanderthals revisited. New York: Springer Verlag. p 38–69. Ruff C. 2010. Body size and body shape in early hominins– implications of the Gona Pelvis. J Hum Evol 58:166–178. Siervogel RM, Demerath EW, Schubert C, Remsberg KE, Chumlea WC, Sun S, Czerwinski SA, Towne B. 2003. Puberty and body composition. Horm Res Paed 60(Suppl 1):36–45. Silbernagl S, Despopoulos A. 1991. Taschenatlas der Physiologie. Stuttgart; New York: Georg Thieme Deuscher Taschenbuch-Verlag. Slice DE. 1998. Morpheus et al.: software for morphometric research. Version Revision 01–01-2000. New York: Department of Ecology and Evolution, State University, Stony Brook. Smith F. 1980. Sexual differences in European Neanderthal crania with special reference to the Krapina crania. J Hum Evol 9:359–375. StatSoft I. 1999. STATISTICA for Windows. Version 99. Tulsa, OK: StatSoft. American Journal of Physical Anthropology 422 M. BASTIR ET AL. Steegmann AJ, Cerny F, Holliday T. 2002. Neandertal cold adaptation: physiological and energetic factors. Am J Hum Biol 14:566–583. Strand-Viðarsdóttir U, O’Higgins P, Stringer C. 2002. A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton. J Anat 201:211–229. Trinkaus E. 2003. Neandertal faces were not long; modern human faces are short. Proc Natl Acad Sci USA 100:8142– 8145. American Journal of Physical Anthropology Wells JCK. 2007. Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol Metabol 21:415–430. Wood BA. 1976. The nature and basis of sexual dimorphism. J Zool Lond 180:15–34. Yokley T. 2009. Ecogeographic variation in human nasal passages. Am J Phys Anthropol 138:11–22. Yokley T, Holton NE, Franciscus RG, Churchill SE. 2009. The role of body mass in the evolution of the modern human nasofacial skeleton. Paleoanthropology A39–A40.