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Common features of sexual dimorphism in the cranial airways of different human populations.

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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: mbastir@mncn.csic.es
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.
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