Basicranial flexion, relative brain size, and facial kyphosis in Homo

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 98:575-593 (1995)
Basicranial Flexion, Relative Brain Size, and Facial Kyphosis in
Homo Sapiens and Some Fossil Hominids
CALLUM ROSS AND MACIEJ HENNEBERG
Biological Anthropology Research Programme, Department of Anatomy
and Human Biology, University of the Witwatersrand, Parktown,
Johannesburg, Republic of South Africa
KEY WORDS
Fossil hominids, Basicranial flexion, Computed
tomography, Brain evolution
ABSTRACT
Comparative work among nonhominid primates has demonstrated t h a t the basicranium becomes more flexed with increasing brain size
relative to basicranial length and a s the upper and lower face become more
ventrally deflected (Ross and Ravosa [19931Am. J. Phys. Anthropol. 91:305324). In order to determine whether modern humans and fossil hominids
follow these trends, the cranial base angle (measure of basicranial flexion),
angle of facial kyphosis, and angle of orbital axis orientation were measured
from computed tomography (CT) scans of fossil hominids (Sts 5, MLD 37/38,
OH9, Kabwe) and lateral radiographs of 99 extant humans. Brain size relative
to basicranial length was calculated from measures of neurocranial volume
and basicranial length taken from original skulls, radiographs, CT scans, and
the literature. Results of bivariate correlation analyses revealed that among
modern humans basicranial flexion and brain sizehasicranial length are not
significantly correlated, nor are the angles of orbital axis orientation and facial
kyphosis. However, basicranial flexion and orbit orientation are significantly
positively correlated among the humans sampled, as are basicranial flexion
and the angle of facial kyphosis. Relative to the comparative sample from
Ross and Ravosa (1993), all hominids have more flexed basicrania than other
primates: Archaic Homo sapiens, Homo erectus, and Australopithecus africanus do not differ significantly from Modern Homo sapiens in their degree
of basicranial flexion, although they differ widely in their relative brain size.
Comparison of the hominid values with those predicted by the nonhominid
reduced major-axis equations reveal that, for their brain sizehasicranial
length, Archaic and Modern Homo sapiens have less flexed basicrania than
predicted. H. erectus and A. africanus have the degree of basicranial flexion
predicted by the nonhominid reduced major-axis equation. Modern humans
have more ventrally deflected orbits than all other primates and, for their
degree of basicranial flexion, have more ventrally deflected orbits than predicted by the regression equations for hominoids. All hominoids have more
ventrally deflected orbital axes relative to their palate orientation than other
primates. It is argued that hominids do not strictly obey the trend for basicranial flexion to increase with increasing relative brain size because of con-
Received October 28, 1994; accepted August 15, 1995.
Address reprint requests to Dr. Callum Ross, Dept. Anatomical
Sciences, Health Sciences Center, SUNY Stony Brook, Stony
Brook. NY 11794-8081.
0 1995 WILEY-LISS. INC.
576
C. ROSS AND M.HENNEBERG
straints on the amount of flexion that do not allow it to decrease much below
90". Therefore, if basicranial flexion is a mechanism for accommodating a n
expanding brain among non-hominid primates, other mechanisms must be
at work among hominids. o 1995 Wiley-Liss, Inc.
Homo sapiens have long been known to
have highly flexed basicrania. Extreme basicranial flexion in humans has been claimed
to provide better balance of the head on the
vertebralcolumn(Wood Jones, 1917;Weidenreich, 1924, 1941; DuBrul, 19501, to create
a pharynx shape suitable for the generation
of vowel sounds used in human speech (Laitman, 1985),to reduce stresses in the anterior
part of the cranial base due to loading of the
jaw joint or occipital condyles (Demes, 1985),
or to be the result of increases in relative
brain size and decreases in the relative size
of the masticatory apparatus (Biegert, 1963;
see review in Ross and Ravosa, 1993). Basicranial flexion has also been invoked a s evidence in support of various hypotheses regarding the taxonomic relationships among
hominoids (Dean and Wood, 1981, 1982,
1984; Shea, 1985). Elucidation of the functional and structural correlates of basicranial flexion is therefore of importance for the
understanding of hominoid cranio-facial evolution.
Previous comparative work on basicranial
flexion in non-hominid primates found no
correlation between the degree of basicranial
flexion and habitual orthograde posture but
confirmed Gould's (1977) suggestion that increases in brain size relative to basicranial
length are correlated with increased basicranial flexion (as indicated by decreases in the
cranial base angle [CBA]) (Ross and Ravosa,
1993). In addition, positive correlations were
found between measures of basicranial
flexion and the orientation ofthe orbital axes
and palate, indicating that a s the basicranium becomes more flexed, the face becomes
more ventrally deflected (i.e., more kyphotic
or klinorhynch).
The present study was carried out to determine whether the degrees of basicranial
flexion and palatal and orbital kyphosis in
hominids follow the trends documented by
Ross and Ravosa (1993) for non-hominid primates. Specifically, we sought to test the fol-
lowing null hypotheses: a ) that hominids
have the degree of basicranial flexion expected for primates with their brain size relative to basicranial length, and b) that hominids have the orbit and palate orientation
expected for primates with their degree of
flexion. If hominids follow the trends of association exhibited by nonhominid primates,
then the same causes of flexion may be postulated; if all or some of the hominids deviate
from these trends, then different mechanisms may be invoked.
MATERIALS AND METHODS
Sample
The sample of Homo sapiens used in this
study consisted of 99 adult skulls from the
Raymond A. Dart Collection of Human Skeletons in the Department of Anatomy and
Human Biology at the University of the Witwatersrand. The specimens were selected to
represent both sexes, a wide size-range and
diverse ethnic origins. An attempt was made
to measure five males and five females from
all the major ethnic groups sampled in the
Dart Collection, with the remaining skulls
chosen to sample specimens of unusual origins (see Table 1).Lateral radiographs of
the skulls were made in the Department of
Radiology, Johannesburg General Hospital.
The measurement techniques employed
here (see below) require fairly complete and
undistorted basicrania, a rare situation in
fossil hominids. Moreover, of those hominids
with complete basicrania, only a small proportion have been scanned by computed tomography, the East African hominids being
the most important exceptions. As a result,
the sample of fossil hominids available for
this study was restricted to Sts 5, MLD 37/
38 (Australopithecus africanus),OH9 (Homo
erectus), and the Kabwe Skull (archaic
Homo sapiens).
Measurements of Sts 5 and MLD 37/38
were taken from computed tomography (CT)
577
HOMINID BASICRANIAL FLEXION
TABLE 1. Composition
of human sample (ethnicity and
sex as recorded in Dart Collection records)‘
Ethnicity
Zulu
Xhosa
Venda
Indian
Tswana
Malawi
Dama
Fingoe
Amazon
Sotho
Ndebele
European
Chinese
Griqua
Bushman
Kalanga
Totals
Unknown
sex
Specimen
Males
5
5
Females
Total
6
5
11
10
3
8
10
5
1
3
4
4
5
5
5
1
1
1
5
5
1
1
1
5
5
8
10
18
TABLE 2. Computed tomography scans used to
take measurements
6
1
3
46
35
1
10
10
8
10
9
1
99
‘Zulu = Zulu-speaking; Xhosa = Xhosa-speaking; Venda = Vendaspeaking; Indian = individuals classified by South African apartheid
laws as Indian (probably related to peoples originating in Indian suhcontinent);Tswana = Tswana-speakingpeoples;Malawi = Malawians;
Dama = from Damaraland in northern Namibia; Fingoe = South
African tribe; Amazon = Amazonian Indian; Sotho = Sotho-speaking
peoples; Ndebele = Ndebele-speaking peoples; European = individuals classified as “White” by South African apartheid laws; Chinese = immigrants from China to South Africa; Griqua = individuals from old frontier community mostly of Khoi-San descent with
European admixture; Kalanga = tribe from Botswana, Zimbabwe,
and northern South Africa.
Sts 5
MLD 37/38
Kabwe skull
OH9
Tape location
Scan numbers
Transvaal Museum
Pretoria, SA
Transvaal Museum
Pretoria, SA
Philips HQ
Best, Netherlands
Philips HQ
Best, Netherlands
41 (mid-sagittal)
32 & 51 (orbit)
5 (mid-sagittal)
All scansL
201 (mid-sagittal)
‘Measurements of mid-sagittal variables were taken from the midsagittal section of a three-dimensional reconstruction of t h e Kabwe
Skull.
(i.e., older) measures. As noted previously,
the advantage of Ross and Ravosa’s measure
of the cranial base angle is that the points
used to define the orientation of the occipital
clivus both lie on the clivus, and those used
to define the orientation of the planum sphenoideum both lie on the planum sphenoideum. Thus, our cranial base angle measures only the relative orientation of the
endocranial surfaces of these two bones,
without the confounding effects introduced
by using points such a s nasion or foramen
cecum which lie off these bones.
Angles. The cranial base angle (CBA) is a n
attempt to quantify the relative orientations
of the endocranial surfaces of the clivus ossis
occipitalis (CO) and the planum sphenoideum (PS)(Fig. 1).The orientation of the
endocranial surface of CO is represented by
a line from basion (B in Fig. 1)to the point on
clivus where dorsum sellae begins to curve
away superiorly (D). This latter point is a n
attempt to estimate the position of the endocranial edge of the spheno-occipital synchrondrosis, which defines the anterior edge
of the occipital clivus. The orientation of PS
is represented by a line from the apex of the
declivity above the sulcus chiasmatis (P) to
the apex of the sloping posterior surface of
the pit in which the cribriform plate is set
Measures
(A). The angle between CO and PS is the
The measures taken in this study are CBA.
those described by Ross and Ravosa (1993).
The angle of facial kyphosis (AFK) meaAlthough a plethora of measures has been sures the Orientation of the palate to CO (Fig.
used in the study of basicranial flexion, we 1).The plane of the palate is represented by
believe these new measures to be more ap- a line between anterior (AN) and posterior
propriate for determining the relative orien- (PN) nasal spines. This line is extended postations of the anterior and posterior portions teriorly to reach the plane of clivus: the angle
of the basicranium than more “traditional” between these lines is the AFK. Identificascans (1.5mm slice thickness) of these fossils
stored on tapes at the Transvaal Museum in
Pretoria. They were displayed on the console
of the CT scanner in the Department of
Radiology, Johannesburg General Hospital,
where measurements were taken. Hard copies of the scans were also made to enable
comparison with the original fossils. CT
scans (1.5 mm slice thickness) of the Kabwe
(Broken Hill) Skull and OH9, in the care of
the Foundation for Hominid Palaeoradiology, were measured on a console a t Philips
Headquarters, Best, and University Hospital, Utrecht, Holland. Table 2 lists the scan
slices used for measurement of fossil hominids.
578
C. ROSS AND M. HENNEBERG
Fig. 1. Diagram illustrating points and planes used to measure cranial base angle (LBA) and angle
of facial kyphosis (AFK). B, basion; D, point where dorsum sellae curves away; P, top of declivity above
sulcus chiasmatis; A, top of slope above cribriform plate; PN, posterior nasal spine; AN, anterior nasal
spine.
tion of the posterior nasal spine on the radiographs was facilitated by comparisons with
the skulls themselves. These comparisons
with the original skulls were performed because in the replications performed to evaluate measurement error, these comparisons
were not made and the measurement error
of the AF'K was higher than that for the other
measures (see below, Table 2).
The angle of orbital axis orientation (AOA)
was measured according to the method defined by Ravosa (1988). The orbital axis is
drawn in the following way (see Fig. 2). On
lateral radiographs, the distance (X) from
the center of the optic canal to the anterior
point of overlap of the orbital roof and the
contour of the anterior cranial fossa (A) was
measured. The point on the inferior orbital
border a t distance (X) was then marked (B)
and a line drawn between point B and point
A. The line AB defines the plane of the orbital aperture. The line bisecting this plane
and passing through the center of the optic
canal is the orbital axis (OA). The angle between OA and CO was measured as AOA
(Fig. 2).
Linear measures. Linear measures of endocranial basicranial length (BL) were taken
Fig. 2. Diagram illustrating points and planes used
to measure angle of orbital axis orientation (AOA). AOA
is the angle between orbital axis (OA) and clivus (CO).
A is point of overlap of the orbital roof and the contour
of the anterior cranial fossa. X is distance from optic
canal to A. B is point on inferior orbital margin at distance X from optic canal.
HOMINID BASICRANIAL FLEXION
579
Fig. 3. Photo of midsagittal CT scan of Sts 5 illustrating positions of planum sphenoideum (PS) and
clivus (CO). The angle between these planes is the CBA.
from the radiographs of the humans (Fig. l ) ,
from the mid-sagittal scans of MLD 37/38
and the Kabwe Skull, from the original of
Sts 5 (Fig. 31, from a cast of OH9 in the
Palaeoanthropology Research Unit at the
University of the Witwatersrand, and from
Maier and Nkini’s (1984) reconstruction of
OH9. (In the latter instance the scale of the
drawing [Maier and Nkini, 1984: Fig. 11 was
assessed by measuring the width of the foramen magnum on the cast and on the drawing.) BL is estimated by measuring three
segments: a) basion to pituitary point (Zuckerman, 19551, b) pituitary point to the posterior point on PS (as defined above), and c)
posterior to anterior point of PS. For each
individual, a, b, and c were summed. The
linear measures taken from each radiograph
were then corrected by multiplying them by
the ratio
prosthion-basion length
measured on the radiopraDh
prosthion-basion length
measured on the skull.
Measurements from scans of Sts 5, MLD
37/38,0H9,
and the Kabwe Skull. Angu-
lar and linear measurements of the basicrania of Sts 5, MLD 37/38, OH9, and the
Kabwe Skull were taken from CT images.
Sts 5. Hard copies of Images 27-55 were
made and the mid-sagittal scan identified as
Image 41 (Fig. 3) by comparison with the
original specimen. To control for slight distortion in the specimen, the mid-sagittal
measurements (CBA and AFK) were also
made on Images 39,40, and 42 for comparison with those taken on Image 41 and found
to differ by, a t most, one degree.
The CBA was measured as shown in Figure 3. Figure 4A illustrates the positions of
CO and PS on the original specimen: Figure
4B illustrates the position of the anterior
edge of PS in more detail (APS).
The AOA used here was defined by Ravosa
(1988) for measurement from lateral radiographs and uses points in parasagittal
planes projected onto the radiograph. Because measurements ofAOA in sts 5 were by
necessity taken from parasagittal CT slices
passing through the optic foramina, some
modification of this technique was necessary.
This was done by measuring the orientation
of CO to the horizontal on Image 41 and the
orientation of the orbital axes to the hori-
580
C. ROSS AND M. HENNEBERG
A
B
Fig. 4. Stereophotos of interior of Sts 5 calvaria illustrating A) position of CO and PS, and B) position
of anterior point on planum sphenoideum ( A P S ) .
I
zontal on Images 32 (left) and 51 (right),
enabling the angles between the orbital axes
and CO to be calculated trigonometrically.
The optic foramen on the right side of Sts
5 is not preserved, so it was necessary to
estimate its position using the optic foramen
on the left side. This was done by positioning
the cursor in the center of the optic foramen
in Image 32 then bringing up Image 5 1 without moving the cursor. Although this technique does not take into account some minor
distortion in the fossil, the results are
deemed acceptable because the measurements obtained from the two sides of the
skull are comparable (Table 5). The mean of
these two values (144.8') was used.
MLD 37138. In this specimen, the anterior portion of planum sphenoideum and
most of the face are missing. Consequently,
it was not possible to measure AOA, AFK,
or BL. Nor was it possible to measure the
CBA using the anteriormost point on PS a s
defined above, a s the pit in which the cribriform plate sits is missing. However, because
a significant portion of PS is preserved, it
was possible to estimate the CBA, yielding
a value not dissimilar to that obtained for
Sts 5 (Table 5).
An estimate of BL in MLD 37/38 was also
attempted. The distances from basion to pituitary point, and from pituitary point to the
posterior edge of PS were measured from the
CT scan. The values for these measurements
are similar to those for Sts 5, so the length
of PS in Sts 5 was used a s the estimate of
PS length used to calculate BL in MLD 37/
38 (Table 5).
OH9. The only skull of Homo erectus for
which scans were available is OH9, the midline basicranium of which is badly damaged,
missing much of the dorsal surface of clivus
and dorsum sellae. Maier and Nkini (1984)
have attempted a reconstruction of the basicranium (redrawn in Fig. 5). The position
of basion can be reconstructed from the outline of the foramen magnum a s only several
millimeters of bone appear to be missing.
The position of tuberculum sellae on the left
side has allowed Maier and Nkini to approximate the position of dorsum sellae; however,
it is possible that dorsum sellae may have
been lower than they suggest. The preserved
HOMINID BASICRANIAL FLEXION
581
Fig. 5. Slightly parasagittal scan of OH9 with reconstruction of clivus by Maier and Nkini (1984).
Redrawn from Maier and Nkini (1984). CO’A’ and CO’B’ represent our estimates of the likely upper
and lower limits possible for the position of CO. MN is the position of CO as measured from Maier and
Nkini’s reconstruction.
portions of tuberculum sellae and lamina cribrosa can be used to reconstruct planum
sphenoideum, although with limited confidence. One estimate of CBA (MN in Fig. 5)
was taken from Maier and Nkini’s (1984)
reconstruction, one was taken from a
slightly modified version of this reconstruction, with the dorsum sellae slightly lower
(CO’B’ in Fig. 5) and one was taken by rough
estimate from the mid-sagittal scan stored
at Philips Headquarters in Best (CO’A’ in
Fig. 5). This latter reconstruction assumes
that basion was further forward than Maier
and Nkini reconstruct it. The three differing
results, listed in Table 5, are presented with
some circumspection. We have not examined
the original skull itself, and would not be
surprised if our estimates were significantly
in error. Consequently, OH9 is given only
cursory treatment in this study.
Kabwe skull. Measurements of the
Kabwe Skull were taken from the mid-sagittal section (CBA, AFK, BL) or parasagittal
section (AOA) of a three-dimensional reconstruction of CT slices stored at Philips. All
points on the midline basicranium used for
measurements in this study are preserved.
The method used for measuring AOA in Sts
5 was applied to the left side of the Kabwe
Skull with the assistance of Prof. Zonneveld.
Volumes. Estimates of overall brain size in
the human sample were made by measuring
the endocranial volume of the skulls with
mustard seed. After plugging up foramina
and holes due to breakage, the neurocranium was filled with mustard seed through
the foramen magnum while gently shaking
the skull from side to side. The skull was
then tapped with a finger and more seed
added. This procedure was repeated until no
more mustard seed would fit into the braincase. The mustard seed was then poured into
a graduated cylinder which was shaken until
the column of seed had a flat surface a t the
top. The volume was then read off the
cylinder.
The volumes of the neurocrania of OH9,
Sts 5, and MLD 37/38 were taken from Holloway (1973a,b). Neurocranial volume in the
Kabwe Skull was obtained from Pycraft
(1928) rather than Holloway (1981) because
Zonneveld’s (pers. comm.) estimate of neurocranial volume in Broken Hill using 3-dimensional reconstruction of the CT slices of
the skull is identical to that obtained by
Pycraft .
Statistical analyses
Reliability of the radiographic methods
and the techniques for taking measurements
582
C. ROSS AND M. HENNEBERG
TABLE 3. Measurement error: Results o f t h e analysis of
variance i n measurements of CBA, AOA, and AFK
repeated fiue times on fiue human skulls (n = 25, k = 51
CBA
AOA
AFK
Mean
Total
variance
Error
variance
Erroritotal
109.04
118.78
123.88
69.14
37.98
35.91
4.02
2.23
4.98
0.0582
0.0587
0.1386
from the radiographs were evaluated by taking five lateral radiographs of each of five
skulls and measuring the CBA, AFK, and
AOA once on each radiograph. The radiographs were all taken on one day; one radiograph for each specimen was measured each
day for five days. One-way analysis of variance (ANOVA)( P < 0.05) indicated that the
variance of the replicate measurements
taken on single individuals is significantly
less than the inter-individual variance. Error variance calculated from the one-way
ANOVA is shown in Table 3.
Descriptive statistics for all measurements taken from Homo sapiens are presented in Table 4. Sample sizes for H. sapiens
are less than 99 because it was not possible
to take measurements from all skulls that
were radiographed. Index of Relative Encephalization 1(IREl)--cube root of neurocranial volume divided by basicranial length
(Ross and Ravosa, 1993)-was calculated for
each individual measured. Descriptive statistics for IREl are also given in Table 4.
The values obtained for the fossil hominids
are presented in Table 5, as are the means
for the same measurements taken from the
great apes.
In order to evaluate the null hypotheses,
Student’s t-tests were used to determine
whether the mean values for Homo sapiens
and the individual variates for the fossil
hominids are significantly different from the
values predicted from the nonhominid primate reduced major-axis (RMA) regression
equations. Formulae for the standard errors
used to calculate 95% confidence limits of the
predicted individual values and the sample
means were taken from Sokal and Rohlf
(1981). RMA equations were used for prediction because we have no reason to believe
that our x-values are measured without error. More importantly, many of our predictions pertain to x-values lying well outside
the range of values used to generate the
equation, a situation in which RMA performs better than least-squares (Draper and
Smith, 1981; Ricker, 1984).
RMA slopes were compared using a computer program written by Tim Cole; y-intercepts were compared using the “quick test”
of Tsutakawa and Hewett (1977). Table 6
lists the RMA equations for nonhominids,
nonhominoids and hominoid primates, along
with the standard errors of b and the y-intercept. Bivariate plots of the comparisons
listed above were created and the RMA lines
for non-hominid primates were added (Figs.
6-9). These lines enable the position of hominids relative to the general nonhominid primate trends to be evaluated. In Figures 7-9,
the RMA for hominoids was also added to
illustrate the divergent trends seen in hominoids. Note that the RMAs for nonhominid
and nonhominoid primates are very similar
(Table 6).
Loess (Lowess) curve-fitting was applied
to the data on CBA and I R E l in order to
describe the nature of the change in CBA
with increasing relative brain size. Being a
nonparametric regression technique, Loess
has the advantage of making fewer assumptions about the form of the relationship be-
TAELE 4. Descriptiue statistics for measurements taken on sample of Homo sapiensl
Homo sapiens
n
Mean
S.D.
Min.
Max.
Neurocranial volume (cc)
CBA (deg.)
AFK (deg.)
AOA (deg.)
Na-S-Ba (deg.)
IRE 1
BL (mm)
92
93
93
93
83
89
94
1,351
111.8
122.2
114.6
134.7
1.65
67.6
148.1
7.43
6.52
6.40
6.09
0.172
6.45
1,050
92
103
102
116
1.36
45.23
1,835
135
140
133
149
2.25
79.3
‘CBA = cranial base angle; AFK = angle of facial kyphosis; AOA = angle of orbital axis orientation; Na-S-Ba = nasion-sella-basion angle;
IREl = index of relative encephalization 1; BL = basicranial length.
583
HOMINID BASICRANIAL FLEXION
TABLE 5. Mean values for measurements on great apes (from Ross, 19931 and values
for measurements on fossil specimens
Neuro
volume
AFK
AOA
(deg.1
BL
(mm)
IRE 1
167.0
161.0
163.0
L = 144.2
R = 145.5
71.62
70.85
77.22
60.67
1.03
1.04
1.02
1.30
110.5
58.80
1.29
99.0
92.7
104.0
128.0
88.92'
88.92
88.92
81.60
1.15
1.15
1.15
1.33
(cc1
CBA
(deg.)
(deg.1
Pongo pygmaeus
Pan troglodytes
Gorilla gorilZa
Sts 5
396.8
398.3
489.6
485.0
135.0
152.0
148.0
114.0
162.0
156.0
150.0
141.0
MLD 37/38
OH9'
(M&N)
(CO'B')
(CO'A)
Kabwe Skull
435.0
1,067.0
1,067.0
1,067.0
1.280.0
n
125.0
127.0
'M&N, estimate of CO onentation taken from Maier and Nkini's (1984) reconstruction; CO'A, estimate of upper limit possible for orientation
of CO; CO'B', estimate of lower hmit possible for onentation of CO.
Estimate of basicranial length based on Maier and Nkini (1984) reconstruction,
TABLE 6. Statistics for RMA regression eauations for nonhominid. nonhominoid. and hominoid urimates
b
n
CBA x IREl
Nonhominid
primates
Nonhominoid
primates
Hominoids
AOA x CBA
Nonhominid
primates
Nonhominoid
primates
Hominoids
AFK X CBA
Nonhominid
primates
Non h omin oid
primates
Hominoids
AOA x AFK
Nonhominid
primates
Nonhominoid
primates
Hominoids
64
58
11
66
60
8
66
60
9
65
59
8
sb
- 132.30
12.776
- 138.92
15.239
-120.83
29.596
277.62
10.868
304.81
12.758
216.51
33.074
1.085
0.1049
1.204
0.8522
0.923
0.2035
-14,037
17.3364
-35.268
18.5827
25.198
29.2802
1.045
0.1138
1.140
0.1130
0.786
0.1861
-23.201
18.7914
-40.924
18.7962
36.670
26.4301
1.026
0.0667
1.050
0.0673
1.419
0.1246
12.145
9.9655
9.402
9.9932
-56.631
18.8118
tween CBA and IREl than standard parametric techniques (Efron and Tibshirani,
1991).
Despite the fact that our measurement
techniques are not ideal for intraspecific
studies (Ross and Ravosa, 19931, the large
size of our human sample and the low errors
r
P
-0.649
***
-0.571
*:i*
-0.677
0.633
***
0.708
**:!:
0.841
***
0.490
***
0.650
***
0.779
0.856
***
0.875
***
0.976
+**
associated with our measurements of the human sample (Table 2) suggest that it would
be of interest to determine whether the nonhominid primate trends discussed in the Introduction hold within humans as a group.
Consequently, RMA equations and Pearson
correlations were computed for the following
C. ROSS AND M. HENNEBERG
584
190
Hylohatids
180
0
Great Apes
170
+
Homo sapiens
4
Australopithecus africanus
160
Kahwe
150
140 I
"\
\u
130
120
110
I00
X
##
90
.8
.6
1
1.2
1.4
1.6
2
1.8
2.2
Index of relative encephalization 1
Fig. 6. Bivariate plot of the cranial base angle (CBA) and index of relative encephalization 1 (IRE11
in primates. The latter variable is calculated as the cube root of neurocranial volumehasicranial length.
The reduced major-axis (RMA) regression line for nonhominid primates is shown. The polygon surrounding the human mean defines the range of values obtained over the human sample
190
8
'3
Q
1
170
Y
's8 -
150 -
Y
2o a9
130
- H F y .
+I-
0
22
110
-
0 Non-hominoid primates
W
GreatApes
+
Homo sapiens
90
70
Hylohatids
0
Australopithecus africunus
-
Nonhominid RMA
1
.
-
-
1
-..
0
1
.
9
-
1
-.
-
1
Kabwe
. . . , . .
Fig. 7. Bivariate plot of the angle of orbital axis orientation (AOA) and the cranial base angle (CBA)
in primates. The reduced major-axes (RMA) for nonhominid and hominoid primates are added. The
polygon surrounding the human mean defines the range of values obtained over the human sample.
bivariate comDarisons within the Homo saRESULTS
piens sample:*CBA vs. IRE1; CBA vs. AOA;
Homo sapiens
CBA VS.AF'K; AOA vs. AF'K. Pearson correlation coefficients were acceDted as signifiDescriptive statistics for the measures
taken o n the human sample are presented
cant at P < 0.05.
~~
585
HOMINID BASICRANIAL FLEXION
180
170
Hylobatids
I0
Great Apes
120
I0
Homo sapiens
Ausfrulopithecus africanus
110
0
I+
6)
$
Kabwe
I
I
I
100
Cranial base angle (degrees)
Fig. 8. Bivariate plot of the angle of facial kyphosis (AFK) and the cranial base angle (CBA) in
primates. The reduced major-axes (RMA) for nonhominid and hominoid primates are added. The polygon
surrounding the human mean defines the range of values obtained over the human sample.
cu
0
90
I
100
I
.
110
"
I
.
120
'
'
I
.
130
.
.
I
.
140
.
~
150
l
'
'
'
160
I
'
'
170
'
I
~
~
'
t
180
Angle of facial kyphosis
(degrees)
Fig. 9. Bivariate plot of the angle of orbital axis orientation (AOA) and the angle of facial kyphosis
(AFK) in primates. The reduced major-axes (RMA) for nonhominid and hominoid primates are added.
The polygon surrounding the human mean defines the range of values obtained over the human sample.
in Table 4. Mean neurocranial volume and
the standard deviation of the sample are
very similar to those estimated for the human species by larger samples (approx.
1,350 cc and 157 cc, respectively [Henneberg,
1990; Tobias, 19941); other sample statistics
obtained in the present study may therefore
also be good estimates of the degree of human variation. Similarly, the values for neurocranial volume obtained for the great apes
586
C. ROSS AND M. HENNEBERG
(Table 5) are comparable with those given
by Tobias (1994).
Figure 6 is a plot of CBA (cranial base
angle) against I R E l (Index of Relative Encephalization 1) with the RMA regression
line for nonhominid primates added. Homo
sapiens has a much larger brain size (estimated by neurocranial volume) relative to
basicranial length than do other primates
(Fig. 6): the mean IREl for humans lies outside the range for nonhominid primates.
Also, a s has long been known, modern humans have more flexed basicrania than
other primates (Fig. 6). The range of values
for the CBA in modern humans extends from
135", equal to the mean for the Pongo sample, to 92" (three standard deviations from
the mean). The correlation between CBA and
IREl that was observed across nonhominid
primates (Ross and Ravosa, 1993) was not
seen within the human sample. One-tailed
t-tests reveal that the mean value for the
cranial base angle in humans is significantly
higher than the mean predicted by the nonhominid RMA.
The entire range of values for the angle of
orbital axis orientation (AOA) recorded for
Homo sapiens lies outside the range of mean
values for other primates: humans have
more ventrally deflected orbital axes than
all other primates (Fig. 7). Modern humans
also have more ventrally deflected orbital
axes than expected for a hominoid with their
CBA, despite the fact that the human mean
was included in the calculation of the hominoid RMA (Fig. 7 ) !However, the mean value
for AOA among humans does not differ significantly from the mean value predicted by
the nonhominid RMA regression equation
(Fig. 7). Within the human sample, the correlation between AOA and CBA was moderate
(r = 0.705) while the resulting RMA line
(r = 0 . 8 4 8 ~+ 19.768) is not significantly
different from the RMA for AOA and CBA
across hominoids.
The mean value for the angle of facial kyphosis (AFK) for the human sample is
equalled or exceeded by the means of all but
four other primates (Figs. 8 and 9). Thus,
modern humans have comparatively ventrally deflected palates. However, the mean
value for the AFK among modern humans
is significantly higher (one-tailed t-test)
than the mean value estimated by the nonhominid RMA equation (Fig. 8).The correlation between AFK and CBA observed in interspecific comparisons across nonhominid
primates (Ross and Ravosa, 1993) is observed within the human sample (r = 0.492)
with the RMA equation (y = 0 . 8 7 6 ~+
24.261) not being significantly different from
that for all hominoids.
Regression of AOA on AFK is illustrated
in Figure 9. One-tailed t-tests reveal that,
for their AFK, humans have more ventrally
deflected orbital axes than predicted by the
nonhominid RMA equation. AOA and AF'K
are not significantly correlated within the
human sample a s they are among nonhominid primates.
Fossil hominids
A. africanus and Archaic Homo sapiens
resemble modern humans in having more
flexed basicrania than non-hominid primates. Two-tailed t-tests suggest that the
CBAs of Sts 5 (114"), MLD 37/38 (126"), and
Kabwe (126") are not significantly different
from the mean for the Homo sapiens sample.
If any of our estimates of the CBA in H.
erectus is correct, then, contra Maier and
Nkini (19841, OH9 also had a degree of
flexion not significantly different from the
human mean.
When CBA is regressed against IREl (Fig.
6) the Kabwe Skull is seen to resemble humans in having a significantly larger CBA
6 e . , a less flexed basicranium) than that
predicted by the nonhominid RMA. The values for the CBA for OH9, Sts 5, and MLD
37/38 do not differ significantly from those
predicted by the RMA equation for nonhominids. There are no significant differences between the slopes or y-intercepts of the RMA
equations for the regression of CBA on IREl
among nonhominid, nonhominoid, or hominoid primates (Table 6). Consequently, only
the RMA for nonhominid primates is shown
in Figure 6.
A. africanus resembles H. sapiens in having comparatively ventrally deflected orbits:
the only primates with smaller AOAs are
Tarsius syrichta (139") and H. sapiens (Fig.
7). Sts 5 has a higher AOA than predicted by
the nonhominid RMA equation (one-tailed ttest), having more dorsally deflected orbital
HOMINID BASICRANIAL FLEXION
587
axes than predicted for a nonhominid pri- tion expected for a nonhominid primate with
mate with its CBA.
their degree of basicranial flexion. The orbit
Comparison of the RMAs for hominoids orientation ofA. africanus is as predicted for
and nonhominoids reveals the slopes to be hominoids with their CBA, but higher than
not significantly different, but the y-inter- predicted for a nonhominid (Fig. 7). Comparcept of hominoids to be significantly higher ison of RMA regression lines indicates that
than that of nonhominoids (Table 6). Thus, hominoids have more dorsally deflected
although the AOA and CBA covary across palates than nonhominoids when CBA is
hominoids in a manner similar to that seen taken into account.
in nonhominoids, hominoids a s a group have
All hominoids have more airorhynch
more dorsally deflected palates relative to palates than predicted for nonhominoids
their CBA than other primates.
(and nonhominids) with their degree of basiFigure 8 illustrates the regression of AFK cranial flexion (Fig. 8).Modern humans have
on CBA. Sts 5, the Kabwe Skull, and the fairly kyphotic palates in comparison with
great and lesser apes resemble modern hu- other primates, however. Comparison of
mans in having more dorsally deflected RMA regression lines indicates that homipalates than predicted by the nonhominid noids have more dorsally deflected palates
RMA. Comparison of the hominoid RMA re- than nonhominoids when CBA is taken
gression of AFK on CBA with the RMA for into account.
nonhominoid primates reveals that the
Hominoids, including humans, have more
slopes are not significantly different (Table ventrally deflected orbital axes for their
6) but that the y-intercept for hominoids is palate orientation than other primates
higher than that for other primates. Thus, (Fig. 9).
hominoids have more dorsally deflected
palates €or their CBA than other primates.
DISCUSSION
As in humans, AOA relative to AF'K in Sts
Basicranial flexion
5 is significantly smaller than that predicted
by the nonhominid RMA equation (Fig. 9).
Humans have long been known to have
Comparison of RMA regressions for homi- extreme degrees of basicranial flexion and
noid and nonhominoid primates reveals that australopithecines have often been assumed
their slopes are significantly different to have a degree of flexion intermediate be( P < 0.05): for the range of values covered tween that of humans and the great apes
by primates, hominoids have more ventrally (e.g., Biegert, 1963). The results of the presdeflected orbital axes for their palate orien- ent study suggest that this is not the case:
tation than other primates.
Australopithecus africanus, represented by
Sts 5 and MLD 37/38, has the degree of basicranial flexion seen in Modern and Archaic
SUMMARY OF RESULTS
Homo sapiens. If our estimates of basicranial
Homo erectus, Australopithecus africanus, flexion in OH9 are correct, then this is also
Archaic and Modern Homo sapiens have true of Homo erectus. These results confirm
more flexed basicrania than other primates. observations by Ashton et al. (1975) that baWhen relative brain size is taken into ac- sicranial flexion measured endocranially is
count, Archaic and Modern Homo sapiens similar in Sts 5 to that in Homo sapiens.
have significantly less flexed basicrania However, previous studies of basicranial
than predicted by the nonhominid RMA. H. flexion using measurements on the exterior
erectus and A. africanus have the degree of of the skull found no similarity between Sts
flexion predicted by the RMA regression 5 and Homo sapiens (Laitman et al., 1979).
equation for nonhominids (Fig. 6).
This suggests that endocranial and exocraModern humans have more ventrally de- nial flexion of the basicranium bear little if
flected orbits than all other primates and, any relationship to each other.
for their CBA, have more ventrally deflected
Although A. africanus, H. erectus, and Arorbits than predicted by the RMA for homi- chaic and Modern humans have similar denoids. However, they have the orbit orienta- grees of basicranial flexion, relative brain
588
C. ROSS AND M. HENNEBERG
size in the four groups is very different: the may select for increased basicranial flexion
humans have a much greater brain size rela- with increasing relative brain size.
If these explanations for the correlation
tive to basicranial length than A. africanus
and H. erectus. In the context of non-human between increasing relative brain size and
primates, A. africanus and H. erectus have increasing flexion are correct, why do huthe degree of flexion for their relative brain mans not obey the nonhominid primate
size predicted by the RMA, but Homo sapiens trend? Basicranial flexion is correlated with
have less flexed basicrania than predicted. orbit and palate orientation, both across all
Thus, anatomically modern humans do not primates and among modern humans, i.e.,
follow the nonhominid primate trend €or ba- increasing basicranial flexion is associated
sicranial flexion to increase with increasing with increased ventral deflection of the orbrain size relative to basicranial length. Be- bital axes and palate relative to clivus. If
fore addressing the deviation of humans humans had the CBA predicted for a primate
from the non-hominid primate trend, why of their relative brain size, and values for
does this trend exist in other primates?
AFK and AOA predicted for a primate with
As noted by Ross and Ravosa (1993), in- that CBA, their faces and basicrania would
creasing flexion of the basicranium effec- be so closely approximated as to occlude the
tively increases the volume of the skull uti- airway and disturb the functional relationlized as neurocranium without increasing ships in the masticatory apparatus. This is
the length of the skull “in a fashion analo- clearly untenable. It would seem that, given
gous to increasing the proportion of a sphere the relationships between basicranial
which is utilized without increasing the flexion and the orientation of the upper and
sphere’s diameter” (Ross and Ravosa, 1993, lower face demonstrated here, basicranial
p. 319). Basicranial flexion thereby enables flexion cannot be reduced much below 90”
the brain to be enlarged without changing without radical changes in the entire craits “spherical” shape and without increasing nial architecture.
the diameter of the skull. This is advantaIt is therefore likely that, because of spageous for two reasons. First, although the tial-packing problems, the degrees of basibrain becomes larger, distances between the cranial flexion seen in A. africanus and H.
different parts of the brain are minimized. erectus are close to the extreme value possiIf the brain is enlarged by becoming longer, ble and that modern humans do not exhibit
then the distance between rostra1 and caudal significantly more flexed basicrania because
poles of the cerebrum, for example, would it would be functionally impossible. This imexpand, increasing the time that it takes for plies that brain expansion in the human linneuronal impulses to travel between the two eage beyond that seen in A. africanus must
points. Given that many brain functions are have been accommodated in the skull via
not localized but are dispersed over various mechanisms other than basicranial flexion.
areas of cortex, this may be an important One possible mechanism is suggested below
functional constraint on brain shape. Sec- (see Facial Orientation).
There are also good reasons for believing
ond, a spherical brain results in a spherical
brain case. Spherical shell structures not that there are upper limits to the angle of
only enclose the greatest amount of volume flexion measured by the CBA. Retroflexion
for a given surface area, but they also pro- of the basicranium would not only limit the
vide greater strength than cylindrical shell amount of space available for the brain, but
structures, enabling them to be thinner- it would also reverse the primary flexure of
walled (Demes, 1985). For example, Demes the brain that occurs during primate ontog(1985) has argued that the thick wall of the eny. Thus, the few values for CBA that exHomo erectus skull may be necessary for ceed 180“ (Cheirogaleus major 181“,Loris
strengthening a skull that is elongated in tardigradus 181”,Alouatta belzebul 186“,A.
shape; the more spherical braincase of Homo palliata 188”, and Pithecia pithecia 182”)
sapiens facilitates a thinner-walled calvaria. probably approach the upper limits for the
Thus, there is reason to suggest that selec- CBA. If this is correct, then the line most
tion for a strong and economical brain case appropriate for describing the relationship
HOMINID BASICRANIAL FLEXION
100 1
0.5
I
I
I
1.O
I .5
2.0
Index of relative encephalization 1
Fig. 10. Plot of cranial base angle (CBA) against neurocranial volumehasicranial length (IRE11 with Loess
(Lowess) regression line added.
between CBA and IRE1 is not a reduced major-axis (or least squares regression), but a
logistic curve with asymptotes of approximately 90" and 180". At present, however,
only the flattening out of the bottom part of
the distribution can be demonstrated. Figure 10 illustrates a Loess regression line fitted to all the data from Figure 6 except OH9,
this fossil being excluded because of its fragmentary condition. The decrease in the slope
of the curve as it approaches Homo sapiens
is apparent. It is notable that the most flexed
basicranium recorded among humans has a
CBA of 92", slightly above the proposed lower
limit of 90".
Facial orientation
When interpreting these results, it is important to note that the angle of orbital axis
orientation, the angle of facial kyphosis, and
the cranial base angle measure the orientation of different planes (orbit, palate, planum
sphenoideum) to the same plane-clivus
ossis occipitalis. Consequently, changes in
the orientation of clivus alone will result in
apparently correlated changes in these
angles. However, changes in the cranial base
angle are not necessarily accompanied by
changes in orbit orientation; across strepsirhines, CBA and AOA are not correlated
589
(Ross and Ravosa, 1993). Moreover, measures of orbit orientation that do not use
clivus as a reference plane confirm that orbit
orientation across haplorhines covaries with
the degree of flexion; the degree of orbital
frontation, or the degree of verticality of the
orbital margins relative to a line from nasion
to inion, covaries with the the CBA across
haplorhines but not strepsirhines (Ross,
1995). Finally, although AOA and AFK covary with each other across primates with a n
RMA slope not significantly different from
1.00, a s expected ifchanges in clivus orientation account for the correlation between the
two (Table 6 ) ,the nature of this relationship
can change; the slope of the hominoid RMA
is significantly different not only from the
nonhominoid line, but also from a slope of
1.00. Thus, although it is possible for
changes in clivus orientation alone to produce correlated changes in the CBA, AOA,
and AFK, it is clear that more complex morphological changes are being described by
our measurements.
Hominoid primates (great apes, lesser
apes, and hominids) follow the general
trends for palate and orbital axis orientation
to covary with basicranial flexion. However,
they generally have more airorhynch faces
(palates and orbits) than other primates, a s
reflected i n the transposition of the hominoid
RMA lines above that for other primates in
Figures 7 and 8. These data support the hypothesis that this is the primitive condition
for hominoids (Shea, 1985).
Humans are a significant exception to
these trends. Their orbits are more ventrally
deflected than is expected for a nonhominid
primate with their degree of palatal kyphosis and more ventrally deflected than expected for a hominoid with their degree of
flexion. However, they do have the palate
orientation expected for a hominoid with
their degree of basicranial flexion. Why do
humans have such ventrally deflected orbits
in comparison with other primates with similar degrees of flexion (i.e., Australopithecus
africanus)? Why do they display the orbit
orientation expected for a non-hominoid primate with their degree of flexion, rather
than that expected for a hominoid?
Brain expansion in the post-australopithecine lineage leading to Homo sapiens proba-
590
C.ROSS AND M.HENNEBERG
bly occurred primarily via addition of mass
to the periphery of the brain, to the neocortex. The brain ofHomo habilis, which is “appreciably” more encephalized than that of
the australopithecines (Tobias, 19871, exhibits “marked transverse expansion of the cerebrum, especially the frontal and parietooccipital parts . . . and increased bulk of the
frontal and parietal lobes” (%bias, 1987, p.
741). We hypothesize that addition of cortex
to the frontal lobes of the brain was accomplished by a n anterior and inferior movement of the frontal pole relative to basicranial and facial structures. As a result, the
orbits became ventrally deflected relative to
the basicranium, explaining why humans
have the value for the orbital axis orientation predicted for non-hominid primates
rather than hominoids. In other words, modern humans have more ventrally deflected
orbital axes than predicted for a hominoid
with their CBA because of the need to accommodate brain expansion without basicranial flexion.
This may also explain why the hominoid
RMA for the regression of AOA on AFK is
steeper than that for nonhominids (Fig. 9).
It was noted above that although palate and
orbit orientation covary across hominoids,
they do so in a manner different from that in
other primates; i.e., hominoids tend to have
more ventrally deflected orbital axes than
nonhominoids with equivalent degrees of
palatal kyphosis. It is possible that this enables brain expansion to be accommodated
via ventral deflection of the upper face, while
the associated ventral rotation of the palate
is minimized to avoid possibly detrimental
effects to the masticatory apparatus and airway, Humans already have one of the most
kyphotic palates relative to clivus orientation of any primates (Fig. 81, confirming Laitman et al.’s (1979) measurements using exocranial landmarks. It is difficult to imagine
how further restriction of the oropharynxdue to approximation of clivus and palatemight be accommodated.
CONCLUSIONS
Gould (1977) hypothesized that increased
brain size relative to basicranial length is
the most important cause of the extreme ba-
sicranial flexion and other “paedomorphic”
features characteristic of the human skull.
Ross and Ravosa (1993) found, as predicted
by Gould‘s hypothesis, that increasing basicranial flexion among nonhominid primates
is significantly correlated with increasing
brain size relative to basicranial length. The
present study demonstrates that living and
fossil hominids do indeed have larger brains
relative to basicranial length than other primates, a s well a s having more flexed basicrania. However, when the values for hominid basicranial flexion are compared with
those predicted by the nonhominid primate
reduced major-axis equation, it is clear that
Archaic and Modern Homo sapiens have less
flexed basicrania than predicted for their relative brain sizes. Moreover, the considerable
variability in relative brain size among hominids is not correlated with differences in the
degree of basicranial flexion.
These results suggest that although
Gould‘s (1977) hypothesis is generally true
across all primates, increased basicranial
flexion in post-australopithecine hominids is
not attributable to increases in relative
brain size. Hominids probably achieved the
most extreme basicranial flexion possible
early in their evolution; subsequent expansion in relative brain size was not accompanied by increases in basicranial flexion. This
suggests that if basicranial flexion serves a s
a mechanism for accommodating a n expanding brain, then brain expansion among
hominids must have been accommodated by
mechanisms other than basicranial flexion.
One possible mechanism is ventral deflection of the upper face relative to both the
basicranium and the palate; another is lateral expansion of the braincase above the
petrous parts of the temporal bone.
Historical changes in patterns of
morphological correlation
Despite the admittedly restricted sample
of fossil hominids used here, we feel that the
patterns of correlation discussed here (and
in Ross and Ravosa, 1993) can be hypothesized to have arisen as the result of certain
evolutionary changes in anthropoid skull
morphology. In Figure 11,these changes are
mapped onto a n accepted phylogeny of the
Hominoidea; their consequences for patterns
HOMINID BASICRANIAL FLEXION
Apes
A. africanus
591
Homo sapiens
0
Lower limit of
Other’ anthropoids
Fig. 11. Phylogeny ofhominoid primates with evolutionary events discussed in the text mapped onto it.
of interspecific and evolutionary correlation
are depicted in the “correlation-line’’ diagram to the right. Extensive approximation
of the bony orbits below the olfactory tract
in the haplorhine stem lineage resulted i n
morphological integration of the orbits and
anterior basicranium (Ross and Ravosa,
1993; Ross, 1994). As a result, interspecific
changes in orbital axis orientation among
anthropoids were accompanied by correlated
increases in basicranial flexion (and vice
versa). Subsequently, the hominoid stem line a g e - o r a predecessor-acquired increased
airorhynchy (dorsal deflection of the face relative to the basicranium), accounting for the
higher y-intercept of the hominoid RMA in
Figure 7 (Shea, 1985, 1988). This is symbolized in the right side of Figure 11 by the
transposition of the hominoid “correlation
line” above that of other anthropoids. It is
notable, however, that the correlation between AOA and CBA still obtains across
hominoids. Increases in flexion in the hominoid lineage continued until the lower limit
for the CBA (90”) was reached, possibly by
some members of the A. africanus popula-
tion. Further increases in relative brain size
in the lineage leading to modern humanswhich could not be accommodated by increased basicranial flexion-were accommodated by ventral deflection of the orbital
axes, giving Homo sapiens the orbit orientation expected for a nonhominid primate with
their degree of basicranial flexion.
If this sequence of events is correct, the
basicranium of Homo habilis should not be
significantly different from that of humans
(or A. africanus) in its degree of flexion.
Whether the increased ventral deflection of
the orbits posited for the humans lineage
had already occurred in H. erectus or H.
habilis remains to be determined. However,
given the expansion of the neocortex that
was well underway in Homo habilis, it might
be expected that this taxon would exhibit
some ventral deflection of the orbits relative
to the basicranium.
If the sequence of events postulated in Figure 11 is correct, then i t is important to explain why hominoids a s a group have more
airorhynch faces than other primates; it is
this increased airorhynchy that enabled
592
C. ROSS AND M. HENNEBERG
Homo sapiens to accommodate subsequent
neural expansion via ventral deflection of
the orbital axes. It is also important to understand how palate and orbit orientation
might become dissociated during evolution;
it is only via this dissociation that humans
could ventrally deflect their orbits without
also ventrally deflecting their palates. Such
questions regarding morphological integration and “disintegration” during hominoid
evolution remain to be addressed.
ACKNOWLEDGMENTS
We thank Robin Van Der Riet for providing
access to the facilities in the Department of
Radiology at Johannesburg General Hospital, Elspeth Kruger for assistance in obtaining images of Sts 5 , and Berneice Eales
for the lateral radiographs of the Dart Collection skulls. Dr. Frans Zonneveld kindly
provided hospitality and assistance in obtaining access to CT scans in the curatorship
of the Foundation for Hominid Palaeoradiology. At the Transvaal Museum, Dr. Francis
Thackeray kindly granted permission to
study Sts 5 and Mr. David Panagos expertly
removed the calotte of Sts 5 . Thanks are
also offered to Brigitte Demes and Charles
Lockwood, whose comments improved the
manuscript; Bill Jungers, who assisted with
Loess regression; and David Strait, for productive discussions on basicranial evolution.
C.R. was supported by a J.J. Smieszek Research Fellowship in the Department of
Anatomy and Human Biology and by a Postdoctoral Research Fellowship from the University of the Witwatersrand. This research
was supported by a SAFRD Research Grant
to M.H.
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