AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 153:52–60 (2014)

Ontogenetic Scaling of the Human Nose in a Longitudinal Sample: Implications for Genus Homo Facial Evolution Nathan E. Holton,1,2* Todd R. Yokley,3 Andrew W. Froehle,4 and Thomas E. Southard1 1

Department Department 3 Department 4 Department 2

of of of of

Orthodontics, The University of Iowa, Iowa City, IA 52242 Anthropology, The University of Iowa, Iowa City, IA 52242 Sociology and Anthropology, Metropolitan State University of Denver, Denver, CO 80204 Community Health, Wright State University, Lifespan Health Research Center, Dayton, OH 45435

KEY WORDS

energetics; allometry; body mass; sexual dimorphism; development

ABSTRACT Researchers have hypothesized that nasal morphology, both in archaic Homo and in recent humans, is influenced by body mass and associated oxygen consumption demands required for tissue maintenance. Similarly, recent studies of the adult human nasal region have documented key differences in nasal form between males and females that are potentially linked to sexual dimorphism in body size, composition, and energetics. To better understand this potential developmental and functional dynamic, we first assessed sexual dimorphism in the nasal cavity in recent humans to determine when during ontogeny male-female differences in nasal cavity size appear. Next, we assessed whether there are significant differences in nasal/body size scaling relationships in males and females during ontogeny. Using a mixed longitudinal sample we collected cephalometric and anthropometric measurements

from n 5 20 males and n 5 18 females from 3.0 to 20.01 years of age totaling n 5 290 observations. We found that males and females exhibit similar nasal size values early in ontogeny and that sexual dimorphism in nasal size appears during adolescence. Moreover, when scaled to body size, males exhibit greater positive allometry in nasal size compared to females. This differs from patterns of sexual dimorphism in overall facial size, which are already present in our earliest age groups. Sexually dimorphic differences in nasal development and scaling mirror patterns of ontogenetic variation in variables associated with oxygen consumption and tissue maintenance. This underscores the importance of considering broader systemic factors in craniofacial development and may have important implications for the study of patters craniofacial evolution in the genus Homo. Am J Phys Anthropol 153:52–60, 2014. VC 2013 Wiley Periodicals, Inc.

Greater body mass and the resulting increased respiratory demands in archaic Homo have been suggested to influence upper respiratory tract morphology. In particular, researchers have underscored the potential effects of these variables on the size of the nasal cavity (Yokley et al., 2009; Bastir and Rosas, 2011; Froehle et al., 2013). Thus, while there is evidence to suggest that the nasal region may be somewhat modularized with regard to other aspects of craniofacial morphology such as the lateral facial skeleton and the dentognathic region (Chierici et al., 1973; Anton, 1989; Ackermann, 2005; Polanski and Franciscus, 2006; Rhode and Arriaza, 2006; Holton and Franciscus, 2008; Mitteroecker and Bookstein, 2008), nasal skeletal form may be more tightly integrated with other components of the respiratory system (e.g., Enlow, 1990; Rosas and Bastir, 2002; Hall, 2005; Bastir, 2008; Yokley et al., 2009; Bastir et al., 2011). The influence of respiratory function on population and taxonomic variation in nasal cavity form is already well established with respect to the effects of climate and the need to properly heat and humidify respired air (Proetz, 1953; Walker et al., 1961; Franciscus and Trinkaus, 1988; Cole, 1992; Franciscus, 1995; Yokley, 2006, 2009; Noback et al., 2011; Sahin-Yilmaz and Naclerio, 2011; Holton et al., 2013). However, the potential influence of oxygen consumption requirements associated with body mass on nasal morphology is less clear. Assessing the developmental and functional integration between the nasal cavity and other components of

the respiratory system with respect to body mass/ventilatory demands is important for developing a more complete understanding of the evolution of human craniofacial morphology and underscores the potential importance of larger systemic factors on variation in craniofacial size in genus Homo evolution (e.g., Bastir, 2008). For example, researchers have hypothesized that larger facial dimensions in archaic Homo are due, in part, to greater nasal cavity dimensions required to facilitate the necessary oxygen intake needed to maintain a larger body mass (Cartmill and Smith, 2009; Yokley et al., 2009; Bastir and Rosas, 2011; Froehle et al., 2013). Consequently, temporal patterns of facial size reduction in genus Homo (e.g., Trinkaus, 2003; Holton and Franciscus, 2008; Pearson, 2008; Maddux and Franciscus, 2009) may be tied, at least in part, to body mass reduction and reduced daily energy requirements. The potential influence of ventilatory demands on variation in nasal cavity size is difficult to test directly in

Ó 2013 WILEY PERIODICALS, INC.

*Correspondence to: Nathan Holton, University of Iowa: Department of Orthodontics S219 Dental Science Building, Iowa City, Iowa 52242, USA. E-mail: [email protected] Received 17 May 2013; accepted 30 September 2013 DOI: 10.1002/ajpa.22402 Published online 31 October 2013 in Wiley Online Library (wileyonlinelibrary.com).

ONTOGENETIC SCALING OF THE HUMAN NOSE

Fig. 1. Scaling of basal metabolic rate (top) and fat-free mass (bottom) in males (gray) and females (black), ages 3 to 21 years. Each data point represents a sample mean obtained from published studies of BMR in children and was originally compiled as part of a meta-analysis by Froehle (2008).

fossil hominins. However, understanding patterns of oxygen consumption and upper respiratory tract morphology in recent humans can be informative with regard to the influence of respiratory demands on nasal cavity size in archaic Homo. For example, relative to body size, recent human males are characterized by a greater airway diameter and increased lung volume when compared to females (Hopkins and Harms, 2004). This is likely tied to well-established patterns of sexual dimorphism in daily energy requirements and oxygen demands in recent human males and females (e.g., Panter-Brick, 2002). Sexual dimorphism in these parameters typically appear during puberty when children begin to exhibit a significant increase in body mass, changes in body composition, and associated changes in oxygen consumption requirements (Bitar et al., 2000; Maynard et al., 2001; Wells, 2007; Fig. 1). If the nasal cavity is developmentally tied to body mass and associated oxygen requirements, one would predict that this relationship is reflected in male-female

53

differences in nasal cavity size. That is, males should exhibit larger nasal cavity dimensions when compared to females (e.g., Enlow, 1990; Rosas and Bastir, 2002; Hall, 2005; Bastir, 2008; Bastir et al. 2011), thus allowing for greater oxygen intake in males. Recent analyses of nasal variation indicate that there are indeed key differences in males and females that are potentially associated with variation in respiratory function and may facilitate greater oxygen consumption in males compared to females. For example, Rosas and Bastir (2002) and Bastir et al., (2011) have documented that across a wide range of population variation in skeletal samples, males are characterized by absolutely and relatively larger internal nasal cavities due, in part, to relatively and absolutely taller nasal airways in males. Similarly, in a living human sample, Hall (2005) documented that males are characterized by both larger external nasal volumes and greater oxygen consumption during nasal breathing when compared to females. While there appears to be a predictable relationship between sexual dimorphism in oxygen consumption and nasal cavity dimensions, the precise nature of this relationship is unclear. However, given that males are characterized by a disproportionate increase in energy and oxygen consumption associated with adolescent changes in body composition (Bitar et al., 2000; Siervogel et al., 2000; Maynard et al., 2001; Wells, 2007; see Fig. 1), male-female differences in the developmental trajectories and ontogenetic scaling of nasal cavity size would be suggestive of some level of integration between the nasal cavity and respiratory demands. Therefore, our goal is to examine the ontogeny of sexual dimorphism of nasal cavity size using longitudinal cephalometric and anthropometric data from the Iowa Facial Growth Study. If nasal cavity size is tied to variation in body size/composition and ultimately energetic requirements (e.g., Enlow, 1990; Bastir, 2008; Yokley et al., 2009; Bastir et al., 2011; Froehle et al., 2013), we make the following predictions. First, male-female differences in nasal cavity size will appear during early adolescence and correspond to the appearance of sexual dimorphism in body composition. Second, since males exhibit a disproportionate increase in fat-free mass and basal metabolic rate relative to body size (Fig. 1), we predict that relative to measures of postcranial skeletal size (e.g., trunk frame size), male nasal cavity size will scale with greater positive allometry when compared to females. Finally, we predict that the manifestation of sexual dimorphism in nasal cavity size will differ from that of overall facial size, which is established early in ontogeny (e.g., Bulygina et al., 2006).

MATERIAL AND METHODS We collected data from a total of n 5 290 longitudinal observations using the Iowa Facial Growth Study housed at The University of Iowa’s Department of Orthodontics. This study consists of individuals of European descent who lived in or near Iowa City, Iowa. At enrollment, children were at least three years of age, and lateral cephalograms and anthropometric data were taken quarterly until age 5 years. From ages 5 to 12 years, records were taken bi-annually, and from 12 to 18 years, records were taken annually. Records were also taken once during early adulthood (on average ca. 26 years of age). The mixed-longitudinal sample we used for our analysis consisted of n 5 20 males and n 5 18 American Journal of Physical Anthropology

54

N. HOLTON ET AL. TABLE 1. Sample composition

Age 3.0–4.0 5.0 7.0 9.0 11.0 13.0 15.0 17.0 20.01 Total

TABLE 2. Measurements used to calculate nasal and facial geometric mean values

Male n

Female n

Total

17 20 20 19 20 17 9 5 16 143

17 18 18 18 18 17 15 10 16 147

34 38 38 37 38 34 24 15 32 290

females, and was selected from the larger growth study sample based on the completeness of the individual radiographic sequences as well as the quality of the lateral cephalograms with respect to our variables of interest (Table 1). Measurements were collected at nine different observations beginning at 3.0 to 4.0 years of age through age 201 years. The sizes of the nasal region and facial skeleton were calculated using a series of measurements collected from lateral cephalograms and anthropometric data (Table 2, Fig. 2), which allowed us to derive composite size measures that incorporated height, length, and breadth dimensions. Nasal size was calculated as the geometric mean of the following internal skeletal and external soft-tissue measurements of the nose: nasal length (pronasale-hormion), nasal floor length (anterior nasal spine-posterior nasal spine), anterior nasal height (nasion-anterior nasal spine), posterior nasal height (hormion-posterior nasal spine), and external nasal breadth (soft tissue alare-alare). Similarly, facial size was calculated as the geometric mean of bizygomatic breadth (soft tissue zygion-zygion), anterior facial height (nasion-mention), posterior facial height (sella-gonion), and facial prognathism (basion-prosthion). All cephalometric measurements were collected from digitized cephalograms using ImageJ (Abramoff et al., 2004) and were corrected for enlargement. To assess ontogenetic scaling of nasal and facial geometric means, we used two measures of body size. Our first measure, sitting height, was selected due to its availability at all ages (i.e., ages 3.0–20.01 years). Second, we used trunk-frame size, which is calculated as the product of sitting height, and bi-iliac breadth (Ruff and Jamison, 2002; Henneberg and Ulijaszek, 2010). Given that bi-iliac breadth was only available for subjects approximately 11.0 years of age and younger in the Iowa Growth Study, we were only able to calculate trunk-frame size for a subset of our sample (i.e., ages 3– 11 years). To examine the ontogenetic trajectories of the nasal and facial geometric means and to determine the age at which sexual dimorphism in these variables begins to appear, we fitted male and female geometric mean values to Gompertz growth curves. The Gompertz growth curve is particularly accurate with regard to modeling the ontogenetic trajectories of skeletal variables (e.g., German et al., 1994; Humphrey, 1998; Pinhasi et al., 2005) and has been used previously to model the ontogeny of nasal and facial size variables (Holton and Franciscus, 2008). With regard to the initial curve parameters we set the slope at 0.2 and the point of inflexion at zero following previous studies (Humphrey, American Journal of Physical Anthropology

Measurements Nasal geometric mean Nasal length Nasal floor length Anterior nasal height Posterior nasal height External nasal breadth Facial geometric mean Bizygomatic breadth Anterior facial height Posterior facial height Facial prognathism

Description

Type

Pronasale-hormion Ans-pns Nasion-ans Hormion-pns Soft tissue alare-alare

Cephalometric Cephalometric Cephalometric Cephalometric Anthropometric

Zygion-zygion Nasion-menton Sella-gonion Basion-prosthion

Anthropometric Cephalometric Cephalometric Cephalometric

1998; Pinhasi et al., 2005; Holton and Franciscus; 2008). Estimated upper asymptote values for the male and female geometric means were calculated as the average geometric mean value in the 20-year age groups. To assess significant differences nasal geometric mean values between males and females at each age group, we used the nonparametric Mann–Whitney U test. We examined sexual dimorphism in the ontogenetic scaling of nasal and facial geometric means first using reduced major axis (RMA) regression. We regressed logtransformed nasal and facial geometric means against log-transformed sitting height and trunk frame size and assessed differences in male and female slopes. We further assessed scaling differences using mixed model ANOVA to compare least-squares (LS) regression slopes by testing for the interactive effects of sex and body size on nasal and facial geometric means.

RESULTS Summary statistics for nasal and facial geometric means are presented in Tables 3 and 4, and the Gompertz growth curves are found in Figures 3 and 4. With regard to the nasal geometric mean, male and female growth trajectories are largely coincident during the early phases of growth with both sexes exhibiting a steady increase in size. By age 11.0, however, there is a divergence in the growth trajectories as evidenced by the significant differences in male and female geometric means from ages 11.0 to 20.01 (P < 0.05). After age 11.0, the female growth curve begins to flatten while males continue to exhibit a steady increase in the nasal geometric mean through age 20.01, thus resulting in increasing sexual dimorphism in nasal size with age. Male and female growth curves exhibit a similar divergence in facial geometric mean values. During adolescence, males continue to exhibit a relatively steady increase in facial geometric mean values, while the female curve begins to flatten. However, in contrast to the nasal geometric mean comparisons, males are characterized by significantly larger facial geometric mean values beginning at age 3.0 years and continuing through age 20.0 years (P < 0.05). The results of our scaling analyses are found in Tables 5 and 6. Our RMA regression results indicate that relative to ln sitting height, the male ln nasal geometric mean scales with greater positive allometry (m 5 0.66) than the female ln nasal geometric mean (m 5 0.55). The results of our mixed model ANOVA indicate that there is a significant difference in scaling when comparing LS

55

ONTOGENETIC SCALING OF THE HUMAN NOSE

Fig. 2. Cephalometric and anthropometric measurement landmarks used to calculate nasal and facial geometric means (see Table 2). 1 5 nasion; 2 5 pronasale; 3 5 anterior nasal spine; 4 5 prosthion; 5 5 posterior nasal spine; 6 5 hormion (which is largely coincident with the posterior-superior aspect of the pterygoid processes); 7 5 sella; 8 5 basion; 9 5 gonion; 10 5 menton; 11 5 zygion; 12 5 soft tissue alare.

TABLE 3. Summary statistics for nasal geometric mean values Male

Female

Age

Mean

SD

Min

Max

Age

Mean

SD

Min

Max

3.0–4.0 5.0 7.0 9.0 11.0 13.0 15.0 17.0 20.01

23.20 23.93 25.27 26.44 27.60 28.54 30.56 31.20 31.42

0.80 0.69 0.92 1.20 1.07 1.29 1.45 1.56 1.14

21.64 22.20 22.50 23.72 24.68 25.92 28.17 28.89 29.50

24.31 25.06 26.66 29.12 29.71 30.51 33.16 32.85 33.45

3.0–4.0 5.0 7.0 9.0 11.0 13.0 15.0 17.0 20.01

22.73 23.63 24.45 25.86 26.55 27.69 28.21 28.61 28.21

0.67 0.65 0.83 0.89 0.76 0.93 0.86 1.23 0.81

21.28 22.38 22.91 24.14 25.42 25.55 26.31 26.73 26.54

23.80 25.01 25.72 27.39 27.96 28.97 29.58 29.96 29.62

TABLE 4. Summary statistics for facial geometric mean values Male

Female

Age

Mean

SD

Min

Max

Age

Mean

SD

Min

Max

3.0–4.0 5.0 7.0 9.0 11.0 13.0 15.0 17.0 20.01

44.92 46.63 48.95 51.54 52.93 54.86 57.73 58.97 60.68

1.26 1.21 1.31 1.43 1.42 1.67 1.97 1.09 1.61

42.36 43.48 46.3 48.95 50.76 52.20 55.42 57.86 58.18

47.24 48.97 51.84 54.21 55.43 58.22 61.84 60.72 63.27

3.0–4.0 5.0 7.0 9.0 11.0 13.0 15.0 17.0 20.01

43.82 44.55 46.86 48.95 50.32 52.44 54.40 53.42 54.83

1.38 1.48 1.81 1.85 1.88 2.14 1.34 1.80 1.78

41.37 41.21 43.07 44.57 46.05 46.37 52.61 50.69 50.26

47.23 47.10 50.82 53.20 54.62 56.33 57.94 55.24 58.47

regression slopes (P < 0.001). Thus, as body size increases during ontogeny, males exhibit a disproportionate increase in the ln nasal geometric mean relative to females (Fig. 5). Similarly, when scaled to ln trunk frame size using our truncated ontogenetic sequences (Fig. 5), the male regression slope (m 5 0.61) is greater than the female regression slope (m 5 0.53). This difference, however, is not statistically significant (P 5 0.084)

according to our ANOVA results, and is likely due to the smaller sample size and reduced range of variation in the truncated sequence. Facial size scaling relationships are illustrated in Figure 6. With regard to ln sitting height, the male regression line falls above the female line suggesting males are characterized by larger ln facial geometric mean values across the entire range of body sizes. RMA slope American Journal of Physical Anthropology

56

N. HOLTON ET AL.

Fig. 3. Gompertz growth curves fitted to nasal geometric mean values for males (black) and females (gray). Asterisks indicate significant differences (P < 0.05) between male and female nasal geometric mean values within a given age group.

Fig. 4. Gompertz growth curves fitted to facial geometric mean values for males (black) and females (gray). Asterisks indicate significant differences (P < 0.05) between male and female facial geometric mean values within a given age group.

values indicate that during ontogeny males (m 5 0.61) scale with greater positive allometry compared to females (m 5 0.56). Our mixed model ANOVA results show that there is a significant difference in scaling based on LS regression slopes. When scaled to ln trunk frame size there is no significant difference in LS regression line slopes (P 5 0.292) and males and females exhibited similar RMA regression slope values (m 5 0.56, m 5 0.53 respectively). Again, the males exhibit larger ln facial geometric mean values across the entire range of ln trunk frame size values and the LS regression yintercept values are significantly different (P > 0.001). The lack of a significant difference in slopes may again be due to the use of a smaller sample that does not span the same range of body size values as ln sitting height.

scale with greater positive allometry in facial size (when scaled to ln sitting height), males exhibit disproportionately larger facial skeletons throughout the entire longitudinal sequence. This result is broadly consistent with previous studies that have also documented early ontogenetic establishment of sexual dimorphism in craniofacial variables. For example, Bulygina et al. (2006) showed in their longitudinal assessment of facial dimorphism that by approximately 3.0 to 4.0 years of age, male and female facial size growth trajectories begin to diverge. In contrast to overall facial size, nasal size exhibits a different ontogenetic pattern of sexual dimorphism in our sample. As with previous research along these lines (Rosas and Bastir, 2002; Bastir et al., 2011), our results show that males are characterized by a larger nasal cavity size when compared to females. While this difference is evident in all age groups, significant differences in nasal size appear during adolescence (11.0 years of age), long after significant differences in overall facial size have been established. Moreover, males and females exhibit significant differences in nasal growth allometries such that males are characterized by greater positive allometry in nasal size during ontogeny. Thus, as body size increases, males exhibit a disproportionate increase in nasal size when compared to females. With regard to allometric scaling of the nasal cavity, patterns of nasal sexual dimorphism largely mirror patterns of ontogenetic variation in variables associated with oxygen consumption and tissue maintenance (see Fig. 1). That is, at smaller body sizes, there is complete overlap of males and females in bivariate space. However, as body size increases, males exhibit a disproportionate increase in nasal cavity size. During puberty, both males and females exhibit significant increases in total body mass. However, while females gain relatively more fat mass, males exhibit a greater increase in fatfree body mass (Bitar et al., 1999, 2000; Maynard et al., 2001; Siervogel et al., 2000; Wells, 2007). During this period, approximately 95% of body weight gain in males is due to increased fat-free mass compared to 85% in females (Bitar et al., 2000). Thus, for a given body size,

DISCUSSION AND CONCLUSIONS Researchers have hypothesized that variation in nasal morphology, both in archaic Homo and in recent humans, is influenced by body mass and associated oxygen consumption demands required for tissue maintenance (Yokley et al., 2009; Bastir and Rosas, 2011; Froehle et al., 2013). The present study contributes to our understanding of this potential developmental and functional dynamic by assessing sexual dimorphism in nasal cavity size in a longitudinal recent human sample in order to (a) assess sexual dimorphism in the nasal cavity in recent humans and determine when during ontogeny male-female differences in nasal cavity size appear; and (b) determine if there are significant differences in nasal/body size scaling relationships in males and females during ontogeny. The results of our analysis suggest that the size of the nasal region and overall facial size exhibit different patterns of sexual dimorphism during ontogeny. With regard to facial size, significant male-female differences were already present in our earliest age group (3.0–4.0 years) indicating that sexual dimorphism is manifest early in development. This difference is also evident in the male and female growth allometries. While males American Journal of Physical Anthropology

57

ONTOGENETIC SCALING OF THE HUMAN NOSE TABLE 5. RMA and LS regression statistics RMA

Male nasal vs. trunk frame Female nasal vs. trunk frame Male facial vs. trunk frame Female facial vs. trunk frame Male nasal vs. sitting height Female nasal vs. sitting height Male facial vs. sitting height Female facial vs. sitting height

2

LS 2

n

Slope

r

95% CI

Slope

r

95% CI

99 91 99 91 142 147 142 147

0.61 0.53 0.56 0.53 0.66 0.55 0.61 0.56

0.76 0.77 0.87 0.88 0.88 0.83 0.93 0.91

0.55–0.67 0.48–0.57 0.52–0.61 0.49–0.57 0.62–0.70 0.51–0.59 0.58–0.63 0.53–0.59

0.54 0.47 0.52 0.49 0.62 0.50 0.59 0.53

0.77 0.78 0.87 0.87 0.88 0.83 0.94 0.91

0.42–0.60 0.42–0.53 0.48–0.57 0.45–0.53 0.59–0.66 0.46–0.54 0.56–0.62 0.51–0.56

TABLE 6. Mixed model ANOVA results Comparison

F

Nasal geometric mean vs. trunk frame Sex 2.66 Trunk frame 636.13 Sex 3 trunk frame 2.97 Nasal geometric mean vs. sitting height Sex 19.64 Sitting height 1791.21 Sex 3 sitting height 21.12 Facial geometric mean vs. trunk frame Sex 0.67 Trunk frame 1275.03 Sex 3 trunk frame 1.12 Facial geometric mean vs. sitting height Sex 6.12 Sitting height 3507.93 Sex 3 sitting height 7.87

P 0.101 >0.001 0.084 >0.001 >0.001 >0.001 0.416 >0.001 0.292 0.014 >0.001 0.005

Significant differences between male and female slopes are in bold.

males are characterized by a disproportionate increase in metabolically expensive lean mass when compared to females. This is reflected by variation in daily energy expenditure (DEE) in males and females during development. At prepubertal, pubertal and post-pubertal stages, males are characterized by increased DEE relative to females (Bitar et al., 1999). However, while there is a 13% difference in DEE between males and females during the prepubertal stage, this difference increases to 27% during the postpubertal stage indicating a disproportional increase in energy expenditure in males during this developmental period. The maintenance of increasing levels of lean body mass requires concomitant increases in oxygen intake. While differences in respiratory anatomy and function are present during early development (Thurlbeck, 1982; Becklake and Kauffmann, 1999), male-female differences become increasingly disparate during adolescence. Bitar et al. (1999), for example, measured VO2 capacity in a cross-sectional sample of males and females and found that during puberty, male peak VO2 increases by approximately 40% in contrast to a 26% increase in females (Bitar et al., 1999). Sexual differences in oxygen consumption are maintained in adulthood as evidenced by greater oral and nasal VO2 (mL/min) in adult males during both rest and periods of exercise (Hall, 2005). Sex differences in oxygen intake and consumption are facilitated by variation in the absolute and relative size of the respiratory tract in males and females (Mead, 1980; McClaran et al., 1998; Rosas and Bastir, 2001; Hopkins

Fig. 5. Nasal geometric mean scaling relative to ln sitting height (top) and ln trunk frame size (bottom) in males (black) and females (gray).

and Harms, 2004; Hall, 2005; Bastir et al., 2011), which may result, at least in part, from differences in ontogenetic scaling of the nasal region. Our results suggest that body mass, and associated tissue maintenance requirements, may be a key contributing factor to variation in the size of the nasal region. While this dynamic is informative with regard to patterns of sexual dimorphism in craniofacial development, American Journal of Physical Anthropology

58

N. HOLTON ET AL.

Fig. 6. Facial geometric mean scaling relative to ln sitting height (top) and ln trunk frame size (bottom) in males (black) and females (gray).

it also has important implications for our understanding of genus Homo evolution. During the Pleistocene, the genus Homo experienced a significant reduction in body mass, with archaic Homo (e.g., H. neanderthalensis, H. heidelbergensis) generally characterized by greater body mass estimates compared to fossil and recent H. sapiens (Ruff et al., 1997, 2005; Churchill et al., 2012; Froehle et al., 2013). While the causal mechanisms associated with this trend in size reduction are incompletely understood, researchers have repeatedly shown that as a result of body mass differences, the basal metabolic rate and DEE of archaic Homo would have exceeded those of early modern and recent H. sapiens (e.g., Sorensen and Leonard, 2001; Aiello and Wheeler, 2003; Churchill, 2006; Cartmill and Smith, 2009; Froehle and Churchill, 2009; Froehle et al., 2013). As a result, archaic Homo would have had substantially higher requisite oxygen demands when compared to modern H. sapiens. Froehle et al. (2013) have estimated that, while at rest, archaic human males would have required an average of 35.0 L O2/day more than Early Upper Paleolithic modern human males. During periods of increased American Journal of Physical Anthropology

physical activity, the oxygen requirements of an archaic human male could have reached more than 70.0 L O2/day. If nasal cavity size is influenced by variation in body mass, then the associated higher oxygen requirements in larger-bodied archaic Homo may have placed constraints on the size of the nasal cavity. Indeed, greater ventilatory demands associated with the maintenance of larger body mass values in archaic Homo have been argued to underlie variation in other aspects of anatomy associated with respiratory function such as larger dimensions of the Neandertal thorax (Franciscus and Churchill, 2002; Churchill, 2006; Gomez-Olivencia et al., 2009, 2012). Similarly, relative to modern humans, archaic Homo exhibits a more capacious nasal cavity, which allows for increased volume of air intake during respiration while decreasing nasal airway resistance (Jelinek, 1994; Franciscus and Churchill, 2002; Yokley et al., 2009; Froehle et al., 2013). Ultimately, this dynamic may be a key-contributing factor to facial size reduction in the genus Homo (Cartmill and Smith, 2009; Yokley et al., 2009; Bastir and Rosas, 2011; Froehle et al., 2013). Given that the midfacial skeleton is largely composed of the nasal cavity, evolutionary changes in nasal cavity size resulting from body mass reduction will be associated with concomitant changes in the size of the midfacial skeleton. Indeed, body mass constraints on nasal cavity size may explain why Neandertals maintain a prognathic midface in spite of a reduced lateral facial skeleton (e.g., Trinkaus, 1987; Franciscus and Trinkaus, 1995). The results of our analysis are consistent with what would be expected if ventilatory needs influence the development of the nasal region (e.g., Yokley et al., 2009; Bastir and Rosas, 2011; Froehle et al., 2013). That is, if the nasal region is responding to respiratory demands associated with the maintenance of expensive tissues, then sexual dimorphism in nasal development and allometric scaling are expected to mirror ontogenetic and allometric patterns previously established for metabolically relevant variables (e.g., Bitar et al., 1999, 2000; Maynard et al., 2001; Siervogel et al., 2000; Wells, 2007). The potential influence of ventilatory demands on the nasal region would underscore the importance of considering broader systemic factors on craniofacial form. Future studies that can relate body composition and associated ventilatory demands directly to nasal morphology along with other aspects of the respiratory system (e.g., postcranial airway dimensions) would serve as an important next step in directly testing hypotheses of nasalmetabolic integration. Ultimately, this would have significant implications for our interpretations of craniofacial evolution and development emphasizing the need to take an organismal approach when assessing at least some aspects of craniofacial morphology (e.g., Bastir, 2008).

ACKNOWLEDGMENTS The authors are grateful to the editors and anonymous reviewers for their valuable comments and suggestions.

LITERATURE CITED Abramoff MD, Magelhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophoton Int 11:36–42. Ackermann RR. 2005. Ontogenetic integration of the hominoid face. J Hum Evol 48:175–197.

ONTOGENETIC SCALING OF THE HUMAN NOSE Aiello LC, Wheeler P. 2003. Neanderthal thermoregulation and the glacial climate. In: van Andel TH, Davies W, editors. Neanderthals and modern humans in the European landscape during the Last Glaciation. Cambridge: McDonald Institute for Archaeological Research. p 147–166. 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. 2008. A systems-model for the morphological analysis of integration and modularity in human craniofacial evolution. J Anthropol Sci 86:37–58. Bastir M, Rosas A. 2011. Nasal form and function in MidPleistocene human facial evolution. A first approach. Am J Phys Anthropol 144:83. Bastir M, Godoy P, Rosas A. 2011. Common features of sexual dimorphism in the cranial airways of different human populations. Am J Phys Anthropol 146:414–422. Becklake MR, Kauffmann F. 1999. Gender differences in airway behaviour over the human life span. Thorax 54:1119–1138. Bitar A, Vernet J, 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 Nutr 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. Cartmill M, Smith FH. 2009. The human lineage. New York: John Wiley Sons. Charles CM. 1930. The cavum nasi of the American Negro. Am J Phys Anthropol 14:177–253. Chierici G, Harrold P, Vargervik K. 1973. Morphogenetic experiments in facial asymmetry: the nasal cavity. Am J Phys Anthropol 14:177–253. 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. p 113–156. Churchill SE, Berger LR, Hartstone-Rose A, and Zondo BH. 2012. Body size in African Middle Pleistocene Homo. In: Reynolds SC, and Gallagher A, editors. African genesis: perspectives on hominid evolution. Cambridge: Cambridge University Press. p. 319–346. Cole P. 1992. Nasal and oral airflow resistors. Arch Otolaryngol Head Neck Surg 118:790–793. Crognier E. 1981. Climate and anthropometric variations in Europe and the Mediterranean area. Ann Hum Biol 8:99– 107. Davies A. 1932. A resurvey of the nose in relation to climate. J R Anthropol Inst 62:337–359. Enlow DH. 1990. Facial growth, 3rd ed. Philadelphia: Saunders. Franciscus RG. 1995. Later Pleistocene nasofacial variation in Western Europe and Africa and modern human origins. Ph.D. Dissertation. New Mexico: University of New Mexico. Franciscus RG, Long JC. 1991. Variation in human nasal height and breadth. Am J Phys Anthropol 85:419–427. Franciscus RG, Trinkaus E. 1988. The Neandertal nose. Am J Phys Anthropol Suppl 75:209–210. Franciscus RG, Trinkaus E. 1995. Determinants of retromolar space presence in Pleistocene Homo mandibles. J Hum Evol 28:577–595. Froehle AW. 2008. Climate variables as predictors of basal metabolic rate: new equations. Am J Hum Biol 20:510–529. Froehle AW, Churchill SE. 2009. Energetic competition between Neandertals and anatomically modern humans. PaleoAnthropology 2009:96–116. Froehle AW, Yokley TR, Churchill SE. 2013. Energetics and the origin of modern humans. In: Smith FH, Ahern JCM editors. The origins of modern humans: biology reconsidered, 2nd ed. Hoboken, NJ: John Wiley and Sons, Inc. p. 285–320. German RZ, Hertweck, DW, Sirianni JE, Swinder DR. 1994. Heterochrony and sexual dimorphism in the pigtailed macaque (Macaca nemstrina). Am J Phys Anthropol 93:373–380. Gomez-Olivencia A, Eaves-Johnson KL, Franciscus RG, Carretero JM, Arsuaga JL. 2009. Kebara 2: new insights

59

regarding the most complete Neandertal thorax. J Hum Evol 57:75–90. Gomez-Olivencia A, Franciscus RG, Couture-Veschambre C, Maureille B, Arsuaga JL. 2012. The mesosternum of the Regourdou 1 Neandertal revisited. J Hum Evol 62:511–519. 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. Henneberg M, Ulijaszek SJ, 2010. Body frame dimensions are related to obesity and fatness: lean trunk size, skinfolds, and body mass index. Am J Hum Biol 22:83–91. Hiernaux J, Froment A. 1976. The correlations between anthropobiological and climatic variables in Sub-Saharan Africa: revised estimates. Hum Biol 48:757–767. Holton NE, Franciscus RG. 2008. The paradox of a wide nasal aperture in cold-adapted Neandertals: a causal assessment. J Hum Evol 55:942–951. Holton NE, Yokley T, Butaric L. 2013. The morphological interaction between the nasal cavity and maxillary sinuses in living humans. Anat Rec 296:414–426. Hopkins SR, Harms CA. 2004. Gender and pulmonary gas exchange during exercise. Exerc Sport Sci Rev 32:50–56. Humphrey LT. 1998. Growth patterns in the modern human skeleton. Am J Phys Anthropol 105:57–72. Maddux SD, Franciscus RG. 2009. Allometric scaling of infraorbital surface topography in Homo. J Hum Evol 56:161–174. Maynard LM, Wisemandle W, Roche AF, Chumlea WC, Guo SS, Siervogel RM. 2001. Childhood body composition in relation to body mass index. Pediatrics 107:344–350. McClaran SR, Wetter TJ, Pegelow DF, Dempsey JA. 1999. Role of expiratory flow limitation in determining lung volumes and ventilation during exercise. J Appl Physiol 86:1357–1366. Mead J. 1980. Dysanapsis in normal lungs assessed by the relationship between maximal flow, static recoil, and vital capacity. Am Rev Respir Dis 121:339–342. Mitteroecker P, Bookstein F. 2008. The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62: 943–958. Noback ML, Harvati K, Spoor F. 2011. Climate-related variation of the human nasal cavity. Am J Phys Anthropol 145:599– 614. Panter-Brick C. 2002. Sexual division of labor: energetic and evolutionary scenarios. Am J Hum Biol 14:627–640. Pearson OM. 2008. Statistical and biological definitions of “anatomically modern” humans: suggestions for a unified approach to modern morphology. Evol Anthropol 17:38–48. Pinhasi R, Teschler-Nicola A, Knaus A, Shaw P. 2005. Crosspopulation analysis of the growth of long bones and the os coxae of three early medieval Austrian populations. Am J Hum Biol 17:470–488. Polanski JM, Franciscus RG. 2006. Patterns of craniofacial integration in extant Homo, Pan, and Gorilla. Am J Phys Anthropol 131:38–49. Proetz AW. 1953. Applied physiology of the nose. St. Louis: Annals Publishing. 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. Rhode MP, Arriaza BT. 2006. Influence of cranial deformation on facial morphology among prehistoric South Central Andean populations. Am J Phys Anthropol 130:462–470. Ruff CB, Trinkaus E, Holliday TW. 1997. Body mass and encephalization in Pleistocene Homo. Nature 387:173–176. Ruff CB, Niskanen M, Junno JA, Jamison P. 2005. Body mass prediction from stature and bi-iliac breadth in two high latitude populations, with application to earlier higher latitude humans. J Hum Evol 48:381–392. Ruff CB, Jamison PJ. 2002. Weight for trunk frame size: an alternative index of fatness in populations of varying body proportions. Am J Phys Anthropol Suppl 34:134. Sahin-Yilmaz A, Naclerio RM. 2011. Anatomy and physiology of the upper airway. Proc Am Thorac Soc 8:31239. Siervogel RM, Maynard LM, Wisemandle WA, Roche AF, Guo SS, Chumlea WC, Towne B. 2000. Annual changes in total

American Journal of Physical Anthropology

60

N. HOLTON ET AL.

body fat and fat-free mass in children from 8 to 18 years in relation to changes in body mass index: the Fels Longitudinal Study. Ann NY Acad Sci 904:420–423. Sorensen MV, Leonard WR. 2001. Neandertal energetics and foraging efficiency. J Hum Evol 40:483–495. Thomson A, Buxton LHD. 1923. Man’s nasal index in relation to certain climatic conditions. J R Anthropol Inst 53:92–122. Thurlbeck WM. 1982. Postnatal human lung growth. Thorax 37:564–571. Trinkaus E. 2003. Neandertal faces were not long; modern human faces are short. Proc Natl Acad Sci USA 100:11231– 11236. Walker JEC, Wells RE, Merrill EW. 1961. Heat and water exchange in the respiratory tract. Am J Med 30:259–267.

American Journal of Physical Anthropology

Weiner JS. 1954. Nose shape and climate. Am J Phys Anthropol 12:615–618. Wells JCK. 2007. Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol 21:415–430. Wolpoff MH. 1968. Climatic influence on the skeletal nasal aperture. Am J Phys Anthropol 29:405–424. Yokley TR. 2006. The functional and adaptive significance of anatomical variation in recent and fossil human nasal passages. Ph.D. Thesis. Durham: Duke University. Yokley TR. 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.

Ontogenetic scaling of the human nose in a longitudinal sample: implications for genus Homo facial evolution.

Researchers have hypothesized that nasal morphology, both in archaic Homo and in recent humans, is influenced by body mass and associated oxygen consu...
333KB Sizes 0 Downloads 0 Views