Journal of Human Evolution 46 (2004) 299–315
A re-evaluation of the metric diversity within Homo erectus
James H. Kidder*, Arthur C. Durband
University of Tennessee, Department of Anthropology, 250 S. Stadium Hall, Knoxville, TN 37996, USA
Received 29 July 2003; accepted 12 December 2003
Abstract
Previous work by several researchers has suggested that the cranial sample from Zhoukoudian possesses a unique
metric pattern relative to the African and Asian specimens assigned to Homo erectus. The current study readdresses this
issue with an expanded fossil sample and a larger and more comprehensive set of cranial measurements. To test the
patterns present in the assemblage, canonical variates analysis was performed using a covariance matrix generated from
the Howells data set. From this, interindividual Mahalanobis distances were computed for the fossils. Random
expectation statistics were then used to measure statistical significance of the Mahalanobis distances. The results show
that the Zhoukoudian hominids exhibit a unique metric pattern not shared by the African and Indonesian crania
sampled. In these tests the Hexian calvaria resembled the African and Indonesian specimens and differed significantly
from the craniometric pattern seen in the Zhoukoudian fossils. The Zhoukoudian specimens are characterized by a wide
midvault and relatively narrow occipital and frontal bones, while the African and Indonesian crania (including Hexian)
have relatively broad frontal and occipital dimensions compared to their midvaults. These results do not suggest that
a multiple-species scenario is necessary to encompass the variation present in the sample. Based on the current evidence
it is more probable that this variation reflects polytypism influenced by environmental adaptation and/or genetic drift.
2003 Elsevier Ltd. All rights reserved.
Keywords: Zhoukoudian; Ngandong; Sangiran; Sambungmacan; Homo erectus; Species; Speciation
Introduction
The number of human species that existed
during the Pleistocene has been the subject of
considerable debate during the past 20 years. The
origins of the current discussion can be traced
back to the 1983 Senckenberg conference, when
Andrews (1984), Stringer (1984), and Wood (1984)
proposed that the fossil material subsumed under
* Corresponding author. Tel.: +1-865-974-4408;
fax: +1-865-974-2686
E-mail addresses: jimpithecus@utk.edu (J.H. Kidder),
adurband@utk.edu (A.C. Durband).
Homo erectus should be split into African and
Asian species. According to this scheme, a number
of autapomorphic features, including the angular
torus, sagittal keel, and the tympanomastoid
fissure, are limited to specimens from Asia. Thus,
the Asian fossils, by virtue of including the type
specimen from Trinil, would retain the species
name H. erectus (Andrews, 1984; Stringer, 1984;
Wood, 1984). The African material, which lacked
these derived features, would be assigned to
H. ergaster, with the KNM-ER 992 mandible as its
type specimen (Groves and Mazák, 1975). Critics
of this view argue that the traits in question have a
0047-2484/04/$ - see front matter 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2003.12.003
300
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
continuous distribution within the H. erectus
sample, as well as other hominid species (e.g.,
Kennedy, 1991; Bräuer and Mbua, 1992).
Multivariate analysis has also been brought to
bear on this issue. Work by Kramer (1993) suggested that the H. erectus sample from Africa and
Asia is metrically homogenous and cannot be
separated into regional groups. Kramer (1993)
examined a relatively large fossil sample, but due
to poor preservation of that sample only three
cranial variables were utilized in his multivariate
study. A number of recent projects by Antón
(2001a, 2002; Antón et al., 2002) have highlighted
some geographic differences in cranial morphology
among the Asian fossils attributed to H. erectus.
However, these studies all utilized a maximum of
four linear cranial measurements (and included
cranial capacity as a fifth variable). This small
number of variables leaves a great deal of potential
variation unexplored. In addition, Antón (2001a,
2002; Antón et al., 2002) did not provide information on the statistical significance of plots
generated by her analyses.
In this paper we reexamine the possibility that
multiple taxa are currently subsumed within
H. erectus. We attempt to quantify the level of
metric variation contained within this temporally
and geographically diverse assemblage using both
an expanded fossil sample and improved cranial
coverage. Kidder (1998) suggested that the Chinese
specimens from Zhoukoudian exhibit a metric
pattern that is not found in the crania from other
sites in Asia and Africa. While he was careful to
note that this seemingly unique metric pattern in
the Chinese specimens probably did not warrant a
separate taxonomic designation for those fossils,
Kidder (1998) did urge further tests of those
results. The current project expands on this earlier
work and attempts to explicate any patterns of
variation that might exist in the fossil sample
currently subsumed under H. erectus sensu lato.
Materials and methods
The sample used for this project is shown in
Table 1. It consists of twenty of the most complete hominid crania commonly described in the
Table 1
Fossil sample used in this project
KNM-ER 3733
KNM-ER 3883
OH 9
Ngandong 1
Ngandong 6
Ngandong 7
Ngandong 11
Ngandong 12
Sangiran 2
Sangiran 17
Pithecanthropus Skull IX (Tjg-1993.05)
Sambungmacan 1
Sambungmacan 3
Sambungmacan 4
Zhoukoudian III
Zhoukoudian V
Zhoukoudian X
Zhoukoudian XI
Zhoukoudian XII
Hexian
literature as belonging to H. erectus (Weidenreich,
1943; Jacob, 1975; Santa Luca, 1980; Rightmire,
1990; Wu and Poirier, 1995; Arif et al., 2001, 2002;
Antón et al., 2002; Baba et al., 2003). This is an
extremely diachronic sample, ranging from
approximately 1.8 Ma for the earliest African
material (Wood, 1991) to possibly as young as
50 Ka for the Ngandong material (Swisher et al.,
1996). A reference sample of known covariance
structure is provided by W.W. Howells’ (Howells,
1973, 1989) modern human data set, which
includes 2354 individuals from a number of
different geographic populations.
For the purposes of this study, Zhoukoudian
Skull III is considered a young adult specimen.
While Black (1929) initially identified this skull as
an adolescent, he later (1930) modified this diagnosis to that of an early adolescent male approximately equivalent to a modern human at twelve
years of age. Weidenreich (1943) essentially agreed
with Black, but gave the specimen a slightly
younger age of eight to nine years. Mann (1981)
disagreed with these assessments, and instead took
the position that this specimen is a young adult
based on the development of muscle markings and
the overall size of the cranium. Antón (2001b)
concurred, and placed Zhoukoudian III at an
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 2
Cranial variables analyzed in this project; definitions for each
measurement can be found in Howells (1973, 1989)
Maximum Cranial Length (GOL)
Maximum Frontal Breadth (XFB)
Maximum Cranial Breadth (XCB)
Biauricular Breadth (AUB)
Biasterionic Breadth (ASB)
Frontal Chord (FRC)
Parietal Chord (PAC)
Occipital Chord (OCC)
older adolescent/young adult developmental age.
Due to the work of Mann (1981) and Antón
(2001b), as well as other results placing this specimen near the Zhoukoudian adults in overall
cranial shape (Durband et al., 2002), the decision
was made to include Zhoukoudian III in the
sample. The recently described “Pithecanthropus
Skull IX” from Sangiran (Tjg-1993.05) is also
included in this analysis, though it should be noted
that sizable inconsistencies exist in the published
measurement sets that are available for this fossil
(e.g., Arif et al., 2001, 2002; Tyler and Sartono,
2001), and additionally the specimen requires a
more concerted effort at reconstruction (Arif et al.,
2002). For this project we will utilize the more
complete set of measurements provided by Arif
and colleagues (Arif et al., 2001) for their most
recent reconstruction of Skull IX.
The variables used in the study are shown in
Table 2, and consist of eight linear cranial
measurements. Due to the fragmentary nature of
the fossil material, variables were chosen based on
their availability on the fossils as well as their
presence in the Howells data set. Measurements
for the fossil sample were obtained from the
literature (Weidenreich, 1943; Santa Luca, 1980;
Rightmire, 1990; Wood, 1991; Wu and Poirier,
1995; Arif et al., 2001; Delson et al., 2001; Baba
et al., 2003).
To test the null hypothesis that the fossil sample
encompasses a single species, the Howells data set
was used to create a pooled covariance matrix
from 28 samples of modern human crania.
Canonical variates and interindividual Mahalanobis distances were then computed for the fossil
samples after Jantz and Owsley (2001). Four dif-
301
ferent tests were run using six, six, seven, and eight
variables, respectively, in order to maximize
coverage of the cranial sample and include less
complete specimens. The variables were transformed using the Darroch and Mosimann (1985)
shape adjustment technique. While Hawks and
colleagues (Hawks et al., 2000) have recently
criticized the use of size adjustment techniques in
craniometric studies of this nature, other workers
have found ample justification for their use
(e.g., Mosimann and James, 1979; Darroch
and Mosimann, 1985; Simmons et al., 1991;
Corruccini, 1992). When employing this methodology, each variable for each individual (row in the
data matrix), is divided by the geometric mean
for all variables. This results in a dimensionless
shape variable. The effect of this technique is to
standardize all crania to one size.
Once the Mahalanobis distances have been
calculated, the fossil crania can be compared to
one another by the use of random expectation
statistics. Through this method, the distance
between pairs of individuals randomly selected
from a population will be distributed as 公(2pⳮ1)
with a variance of 1, where p is the number of
dimensions (Defrise-Gussenhoven, 1967). This
random expectation statistic can be used to determine whether the distance between the fossils
exceeds that expected between individuals drawn
from the Howells data set (Jantz and Owsley,
2001). A distance greater than 1.65 standard deviations above the random expectation value reflects
statistical significance by a one-tailed test (Jantz
and Owsley, 2001). While a modern human reference sample might not be ideal for testing distances
between fossil crania, due to the constraints
imposed by the relatively small fossil sample available this is currently the only alternative. Indeed,
the Howells data set thus provides one of the best
data sets that can be applied to this problem.
Results
The first analysis consists of six variables and
includes sixteen fossil crania (Table 3). This set of
measurements was chosen in an effort to include
Ngandong 6 and OH 9 in the analysis. The results
of this test are plotted in Fig. 1, and the distances
302
Analysis 1
Fossils
Sangiran 17
Pithecanthropus IX
Ngandong 1
Ngandong 6
Ngandong 7
Ngandong 11
Ngandong 12
Sambungmacan 3
Sambungmacan 4
KNM-ER 3733
KNM-ER 3883
OH 9
Zhoukoudian III
Zhoukoudian XI
Zhoukoudian XII
Hexian
Analysis 2
Measurements
GOL
XCB
AUB
ASB
FRC
OCC
Fossils
Sangiran 2
Sangiran 17
Pithecanthropus IX
Ngandong 1
Ngandong 7
Ngandong 11
Ngandong 12
Sambungmacan 3
Sambungmacan 4
KNM-ER 3733
KNM-ER 3883
Zhoukoudian III
Zhoukoudian V
Zhoukoudian XI
Zhoukoudian XII
Hexian
Analysis 3
Measurements
GOL
XCB
XFB
AUB
ASB
OCC
Fossils
Sangiran 17
Pithecanthropus IX
Ngandong 1
Ngandong 7
Ngandong 11
Ngandong 12
Sambungmacan 1
Sambungmacan 3
Sambungmacan 4
KNM-ER 3733
KNM-ER 3883
Zhoukoudian III
Zhoukoudian X
Zhoukoudian XI
Zhoukoudian XII
Hexian
Analysis 4
Measurements
GOL
XCB
XFB
AUB
ASB
FRC
PAC
Fossils
Sangiran 17
Pithecanthropus IX
Ngandong 1
Ngandong 7
Ngandong 11
Ngandong 12
Sambungmacan 3
Sambungmacan 4
KNM-ER 3733
KNM-ER 3883
Zhoukoudian III
Zhoukoudian XI
Zhoukoudian XII
Hexian
Measurements
GOL
XCB
XFB
AUB
ASB
FRC
PAC
OCC
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 3
Fossil samples and cranial measurements used in multivariate tests
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
303
Fig. 1. Canonical variate plot of subset 1.
obtained are shown in Table 4. In this test, clear
separation exists between the Zhoukoudian crania
and the rest of the sample along the first canonical
variate. The only non-Chinese specimen grouping
with the Zhoukoudian fossils in this analysis is
Sambungmacan 3. The first variate accounts for
38.3% of the variance in this test, and is primarily
influenced by a high negative loading on biauricular breadth and a positive loading on maximum
cranial breadth. The second canonical variate
accounts for a further 33.6% of the variation
present in this sample and is primarily driven by a
high positive loading on biasterionic breadth and a
high negative loading on frontal chord. Thus, the
analysis separates crania with relatively broad
midvaults (the Zhoukoudian crania) from those
with relatively narrower midvaults (African and
Indonesian crania) along variate 1, while variate 2
separates skulls with relatively broad occipitals
and relatively short frontals from those with narrower occipital breadths and longer frontal chords.
The Mahalanobis distances generated by this
test, provided in Table 4, show two clear tendencies. First, the distances among the Zhoukoudian
crania are not statistically significant, indicating
similar cranial shape despite the potential time
depth at this site (Grün et al., 1997; Shen et al.,
2001). Secondly, the African and Indonesian
samples do not show a consistent pattern of significant distances from one another, though nearly
all of these crania are significantly different from
all of the Zhoukoudian fossils. The only exceptions
to this pattern are Pithecanthropus Skull IX and
Hexian, both of which show significant distances
to all but three other crania in the analysis, and
Ngandong 12 and KNM-ER 3883, which are
significantly different from only three other
crania in the analysis. Sambungmacan 3 is also an
304
Sang17
PithIX
Ngan1
Ngan6
Ngan7
Ngan11
Ngan12
Sam3
Sam4
ER3733
ER3883
OH9
ZHIII
ZHXI
ZHXII
Hexian
Sang17
PithIX
Ngan1
Ngan6
Ngan7
Ngan11
Ngan12
Sam3
Sam4
ER3733
ER3883
OH9
ZHIII
ZHXI
ZHXII
Hexian
0.000
6.404
4.243
3.928
2.589
3.155
2.823
4.246
3.836
5.125
2.456
3.868
4.742
6.092
6.822
5.324
0.000
4.625
4.336
5.127
3.656
5.449
7.389
5.768
7.563
5.891
5.950
6.826
6.191
6.793
9.821
0.000
4.817
2.610
2.202
4.396
6.344
3.795
6.178
4.197
5.998
7.277
7.660
8.326
7.437
0.000
3.815
3.178
2.382
5.665
5.325
4.992
4.117
3.268
4.907
5.203
6.388
7.554
0.000
2.418
2.308
4.068
2.658
4.089
2.028
4.610
4.974
5.642
6.445
5.407
0.000
3.385
5.763
3.501
5.867
3.304
4.161
5.799
6.340
7.115
7.181
0.000
3.818
4.181
3.157
2.617
3.701
3.989
4.634
5.783
5.625
0.000
5.498
4.959
4.222
6.397
3.954
4.088
4.200
5.982
0.000
4.879
1.937
4.514
5.063
6.250
7.090
4.657
0.000
3.769
5.246
4.833
5.635
6.979
4.334
0.000
3.389
3.719
5.175
6.168
4.067
0.000
4.042
5.646
6.951
6.080
0.000
2.486
3.613
5.663
0.000
1.701
7.587
0.000
8.550
0.000
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 4
Mahalanobis distances obtained for subset 1. Distances >4.960 are statistically significant at the P=0.05 level and are shown in bold type
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
305
Fig. 2. Canonical variate plot of subset 2.
exception to this pattern, exhibiting similarities to
the Zhoukoudian fossils based on these six cranial
measurements.
The second analysis consists of six variables and
includes sixteen fossil crania (Table 3). This analysis was designed to include Zhoukoudian V and
Sangiran 2. The results of the test are plotted in
Fig. 2, and the Mahalanobis distances obtained are
shown in Table 5. As in the previous six-variable
test, the Zhoukoudian crania and the remainder of
the sample separate along the first canonical variate. Here, this variate accounts for 44.3% of the
variation and is driven by high negative loadings
on maximum frontal breadth and biasterionic
breadth and a high positive loading on biauricular
breadth. Variate 2 accounts for 32.5% of the
remaining variation, and is influenced by a high
negative loading on maximum cranial breadth.
Thus, breadths of the frontal and the occipital sort
the crania along variate 1, while maximum cranial
breadth drives the distribution seen on variate 2.
The Mahalanobis distances obtained from
this analysis, displayed in Table 5, show a clear
separation between the Chinese grouping and the
African and Indonesian specimens. Once again,
the Zhoukoudian crania show no statistically significant distances from one another, though each
shows several significant distances from the nonChinese fossils. The African and Indonesian
samples group together to the exclusion of the
Chinese fossils, with the notable exception of
Pithecanthropus Skull IX, which is statistically
significantly distant from every other fossil in the
analysis. As with the previous six-variable test,
Ngandong 12 and KNM-ER 3883 show the greatest similarity to the overall sample, differing significantly from only two and five other crania,
respectively. Finally, Hexian continues to group
306
Sang2
Sang17
PithIX
Ngan1
Ngan7
Ngan11
Ngan12
Sam3
Sam4
ER3733
ER3883
ZHIII
ZHV
ZHXI
ZHXII
Hexian
Sang2
Sang17
PithIX
Ngan1
Ngan7
Ngan11
Ngan12
Sam3
Sam4
ER3733
ER3883
ZHIII
ZHV
ZHXI
ZHXII
Hexian
0.000
5.550
5.959
3.406
3.394
4.206
4.537
7.131
1.616
6.774
2.186
5.283
5.495
6.751
7.548
4.531
0.000
8.131
4.529
3.074
3.511
3.525
4.116
4.858
4.598
3.898
6.189
5.761
7.095
8.014
4.646
0.000
5.439
6.145
5.011
6.056
9.243
5.768
8.924
5.871
6.276
5.300
6.150
6.925
9.504
0.000
2.423
2.033
3.918
6.863
2.904
5.570
3.395
6.771
6.351
7.476
8.550
5.738
0.000
2.425
2.172
4.550
2.616
3.809
1.989
5.146
5.202
5.872
6.951
3.991
0.000
3.291
6.092
3.476
5.607
3.283
5.954
5.051
6.561
7.604
6.137
0.000
4.357
4.236
3.832
2.735
4.342
4.413
4.891
6.113
4.884
0.000
6.203
3.534
5.141
5.506
6.219
5.524
6.224
4.750
0.000
6.048
1.928
5.141
5.277
6.272
7.060
4.347
0.000
5.293
7.053
7.697
6.986
8.075
4.855
0.000
3.829
4.068
5.207
6.115
3.766
0.000
2.233
2.334
2.810
6.097
0.000
3.353
3.867
7.105
0.000
1.327
7.417
0.000
8.136
0.000
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 5
Mahalanobis distances obtained for subset 2. Distances >4.960 are statistically significant at the P=0.05 level and are shown in bold type
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
307
Fig. 3. Canonical variate plot of subset 3.
consistently with the African and Indonesian
specimens and shows statistically significant distances from the Zhoukoudian fossils, including
Zhoukoudian V.
The third analysis examines seven variables
on a sample of sixteen fossil crania (Table 3)
and was designed to include Sambungmacan 1 and
Zhoukoudian X. Results are plotted in Fig. 3, and
the Mahalanobis distances generated are shown in
Table 6. As with the prior two analyses, the
African and Indonesian crania sampled are widely
separated from the Chinese specimens along the
first canonical variate. Variate 1 accounts for
43.2% of the variation with high negative loadings
on biauricular breadth and maximum cranial
length and high positive loadings on maximum
frontal breadth and biasterionic breadth. Variate 2
provides an additional 29.4% of the variation and
is driven by a high negative loading on biauricular
breadth, a high positive loading on frontal chord,
and a moderate positive loading on maximum
cranial breadth. Thus, as in the first two analyses,
the crania are separated by the breadths of the
frontal, occipital, and midvault.
The Mahalanobis distances for this analysis,
shown in Table 6, are broadly similar to those
obtained in the earlier tests. The Zhoukoudian
crania show no significant distances among themselves, while each is significantly separated from
the majority, or even all, of the remaining fossils
tested. The African and Indonesian samples show
a general overall homogeneity with the notable
exceptions of Sambungmacan 3 and Pithecanthropus Skull IX, each of which is significantly distant
from virtually all of the specimens examined from
every region.
The fourth analysis examines eight variables
on a sample of fourteen fossil crania (Table 3).
308
Sang17
PithIX
Ngan1
Ngan7
Ngan11
Ngan12
Sam1
Sam3
Sam4
ER3733
ER3883
ZHIII
ZHX
ZHXI
ZHXII
Hexian
Sang17
PithIX
Ngan1
Ngan7
Ngan11
Ngan12
Sam1
Sam3
Sam4
ER3733
ER3883
ZHIII
ZHX
ZHXI
ZHXII
Hexian
0.000
8.112
4.729
2.869
3.604
3.024
3.883
3.483
4.959
4.333
4.038
6.330
6.393
7.148
7.847
5.515
0.000
5.413
6.255
4.939
6.133
5.126
9.203
6.016
9.500
6.220
6.942
6.818
6.513
6.877
10.492
0.000
2.669
2.320
4.275
3.050
6.642
3.862
6.685
4.344
7.568
7.694
8.017
8.581
7.466
0.000
2.542
3.079
2.425
4.390
3.008
5.457
2.803
5.755
6.010
6.819
7.326
5.372
0.000
2.644
2.119
5.836
3.761
5.451
3.607
6.331
6.463
6.460
7.291
7.253
0.000
1.870
5.320
3.524
4.354
2.225
4.627
5.806
5.146
6.281
5.879
0.000
5.640
2.192
5.059
1.796
4.896
5.926
5.276
6.181
6.051
0.000
6.175
6.331
5.453
6.241
5.071
7.039
6.953
6.068
0.000
5.116
1.812
5.065
6.767
5.917
6.792
4.984
0.000
4.763
7.133
8.727
7.361
8.783
5.303
0.000
3.890
5.849
5.133
6.096
4.555
0.000
3.910
3.153
3.741
6.346
0.000
4.266
3.331
8.487
0.000
2.022
8.418
0.000
9.180
0.000
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 6
Mahalanobis distances obtained for subset 3. Distances >5.276 are statistically significant at the P=0.05 level and are shown in bold type
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
309
Fig. 4. Canonical variate plot of subset 4.
Results are plotted in Fig. 4, and the Mahalanobis
distances generated are shown in Table 7. Not
surprisingly, the Zhoukoudian crania continue to
cluster by themselves and are widely separated
from the African and Indonesian samples
along the first canonical variate (with the notable
exception of Pithecanthropus Skull IX). Variate 1
accounts for 39.2% of the variation and is driven
by moderate negative loadings on maximum
cranial length and biauricular breadth, and high
positive loadings on maximum frontal breadth
and biasterionic breadth. Variate 2 accounts for
another 31.6% of the variation and is influenced by
a high negative loading on biauricular breadth, a
high positive loading on frontal chord, and a
moderate positive loading on maximum cranial
breadth. This plot is particularly noteworthy
because the Zhoukoudian crania separate from the
majority of the African and Indonesian crania on
both axes, unlike the earlier tests where separation
was manifested primarily along the first canonical
variate.
The Mahalanobis distances generated by this
test, shown in Table 7, generally mirror those
of the previous three examinations. The
Zhoukoudian crania group neatly by themselves
and share statistically significant distances from
virtually all of the African and Indonesian specimens. And, as before, no consistent pattern of
significant distances separates the African and
Indonesian samples from one another, aside from
Pithecanthropus Skull IX and KNM-ER 3733,
which are statistically significantly distant from all
but two other non-Chinese crania in the analysis.
Hexian is also notable in being statistically significantly distant from all but three other specimens,
including all of the Zhoukoudian skulls examined.
The status of Ngandong 12 and KNM-ER 3883 is
310
Sang17
PithIX
Ngan1
Ngan7
Ngan11
Ngan12
Sam3
Sam4
ER3733
ER3883
ZHIII
ZHXI
ZHXII
Hexian
Sang17
PithIX
Ngan1
Ngan7
Ngan11
Ngan12
Sam3
Sam4
ER3733
ER3883
ZHIII
ZHXI
ZHXII
Hexian
0.000
8.354
4.909
3.389
3.727
3.635
4.793
5.142
5.439
4.142
6.601
7.517
8.271
5.815
0.000
5.531
6.432
5.152
6.367
9.687
6.314
9.944
6.399
7.125
6.742
7.147
10.771
0.000
2.965
2.503
4.574
7.318
4.113
7.290
4.459
7.781
8.266
8.891
7.715
0.000
3.215
3.079
4.754
3.778
5.686
3.162
5.857
6.868
7.446
5.520
0.000
3.480
6.895
3.893
6.538
3.738
6.671
6.935
7.804
7.626
0.000
5.486
4.397
4.568
2.861
4.766
5.199
6.383
6.055
0.000
7.343
6.308
6.279
6.580
7.131
7.092
6.468
0.000
6.443
2.022
5.517
6.540
7.429
5.458
0.000
5.697
7.482
7.515
8.950
5.741
0.000
4.126
5.504
6.491
4.803
0.000
3.268
3.889
6.496
0.000
2.042
8.591
0.000
9.401
0.000
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 7
Mahalanobis distances obtained for subset 4. Distances >5.565 are statistically significant at the P=0.05 level and are shown in bold type
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Table 8
Measure of biasterionic breadth relative to biauricular
breadth, determined by the formula ASB/AUB
Sangiran 2
Sangiran 4
Sangiran 10
Sangiran 12
Sangiran 17
Ngandong 1
Ngandong 6
Ngandong 7
Ngandong 11
Ngandong 12
Sambungmacan 1
Sambungmacan 3
Sambungmacan 4
Average=
0.960
1.000
0.952
0.893
0.957
0.977
0.913
0.947
0.933
0.933
0.927
0.881
0.931
0.939
ER 3733
ER 3883
OH 9
Average=
Zhoukoudian
Zhoukoudian
Zhoukoudian
Zhoukoudian
Zhoukoudian
Average=
Table 9
Measure of maximum frontal breadth relative to biauricular
breadth, determined by the formula XFB/AUB
0.960
0.930
0.911
0.934
III
V
X
XI
XII
311
0.837
0.835
0.782
0.790
0.762
0.801
Sangiran 2
Sangiran 17
Ngandong 1
Ngandong 7
Ngandong 11
Ngandong 12
Sambungmacan 1
Sambungmacan 3
Sambungmacan 4
Average=
0.810
0.900
0.923
0.879
0.910
0.844
0.847
0.851
0.840
0.867
ER 3733
ER 3883
Zhoukoudian
Zhoukoudian
Zhoukoudian
Zhoukoudian
Zhoukoudian
Average=
0.920
0.814
III
V
X
XI
XII
0.720
0.754
0.748
0.741
0.715
0.736
scores and are higher than those obtained for the
Zhoukoudian fossils.
Discussion
consistent with the previous tests and show the
fewest number of statistically significant distances
from other fossils in the analysis.
To further examine and explain these significant
differences in cranial shape, a simple formula
of biasterionic breadth/biauricular breadth was
applied to a sample of 13 Indonesian, three
African, and five Zhoukoudian fossils listed in
Table 8. The ratios indicate that the cranial vault
does not narrow appreciably at the occipital in
the African or Indonesian samples, indeed the
samples have virtually identical means, but the
Zhoukoudian occipitals are considerably narrower. It is also noteworthy that there is no overlap
between the range of the Chinese crania and those
from Africa and Indonesia. The Chinese and
Indonesian means are significantly different at the
P=0.005 level using a two-tailed t-test. When
frontal breadth is evaluated relative to biauricular
breadth, the Zhoukoudian crania are again found
to show a different pattern than that obtained for
the African and Indonesian samples (Table 9).
Again, there is no overlap between the Chinese and
the African and Indonesian samples and the means
are significantly different at the P=0.005 level using
a two-tailed t-test. While the Hexian cranium is not
included in those tables, that specimen shows
ratios of 0.986 for ASB/AUB and 0.819 for
XFB/AUB. Both of those scores much more
closely resemble the African and Indonesian
The results of this study concur with those of
Kidder (1998), Kidder and Durband (2000), and
with recent work by Antón (2001a, 2002; Antón
et al., 2002) suggesting that the crania from
Zhoukoudian are characterized by a unique metric
pattern not found in the crania from Africa or
Indonesia. The addition of a test for statistical
significance, which was lacking in most of the
previous projects, allows additional weight to be
placed on these findings as well. The Zhoukoudian
specimens are distinguished by very large biauricular breadths and relatively small frontal and
biasterionic breadths, while specimens from
Africa and Indonesia have frontal, midvault, and
occipital dimensions that are more similar in
breadth. This latter pattern of consistently broad
cranial dimensions apparently persisted throughout the considerable time depth of this fossil
sample, except at the site of Zhoukoudian. We also
found that the Zhoukoudian pattern does not
extend to the specimen from Hexian, which instead
exhibits a craniometric pattern that is much more
similar to that seen in Africa and Indonesia.
Thus, it would appear that the craniometric pattern seen throughout much of the Pleistocene was
essentially static. Beginning with the Koobi Fora
crania at approximately 1.8 Ma, a consistent pattern of relatively broad frontal and occipital dimensions as compared to maximum cranial breadth (or,
312
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
conversely, relatively narrow maximum breadth as
compared to frontal and occipital dimensions)
emerged and remained the norm in both Africa and
much of Asia, including the late Ngandong crania.
We cannot state with any certainty whether this
craniometric pattern is primitive or derived in comparison to the immediate ancestors of H. erectus,
whomever they may be, though Antón (2002: 318)
posited that a relatively broad posterior vault is
“liable to be a primitive trait.” However, at the site
of Zhoukoudian a derived pattern compared to that
seen in the remainder of the sample is apparent.
This Zhoukoudian pattern consists of frontal and
occipital dimensions that are narrow relative to
maximum cranial breadth (or a relatively broad
maximum breadth compared to frontal and occipital dimensions) and it consistently separates these
particular fossils from the rest of the H. erectus
sample.
The relatively compressed degree of variation
seen in the Chinese sample is noteworthy. None of
the Zhoukoudian fossils was significantly separated from another specimen from that site in any
of the multivariate analyses, and in most cases the
Mahalanobis distances did not exceed the expected
value for a single biological population. Considering the potential time depth present in the
Zhoukoudian assemblage (Grün et al., 1997; Shen
et al., 2001) the consistency of the metric pattern is
unexpected. A greater degree of variation was
observed in the African and Indonesian samples,
with a number of significant distances generated
between those specimens (approximately one-third
of the distances generated between African and
Indonesian fossils were statistically significant in
the eight variable analysis, for example). However,
this variation is not patterned geographically.
Indeed, in each of the four multivariate analyses
crania from the same site (Koobi Fora and
Sambungmacan) were significantly separated from
one another. The underlying causes of the pronounced variation in the African and Indonesian
samples are not yet clear. They could be attributable to temporal variation or perhaps even reflect
some component of sexual dimorphism. These
explanations are unlikely to suffice for the clear
pattern of differences from the Zhoukoudian
sample, as the Chinese specimens are likely inter-
mediate in age between the earlier African and
Indonesian material and the later Ngandong
sample (Swisher et al., 1996; Grün et al., 1997;
Shen et al., 2001; Antón, 2002). In addition, both
sexes are almost certainly represented in the
Zhoukoudian cranial sample utilized in this study
(Weidenreich, 1943; Mann, 1981).
The profound differences seen between the
Zhoukoudian sample and the Hexian cranium are
also intriguing. This separation has been previously noted by Antón (2001a, 2002; Antón
et al., 2002) and Durband and colleagues
(Durband et al., 2002). Etler (1994: 112a) suggested the possibility that H. erectus from
Zhoukoudian represents a “cold-adapted racial
variation within the population structure of middle
Pleistocene east Asia.” Hexian, on the other hand,
is not associated with faunal elements that would
indicate a cold climate (Etler, 1994). The hypothesis that the Zhoukoudian hominids potentially
reflect a more cold-adapted morphology is worthy
of future study (see Antón [2002] for a more
extensive discussion of this issue).
The position of Zhoukoudian III in these
examinations is worthy of mention. As noted
earlier, some workers have treated it as a subadult
(Black, 1929, 1930; Weidenreich, 1943). Our study
places it very close to the other specimens from this
site and would suggest that Skull III had
approached adulthood at least in terms of its
craniometric pattern. These results would support
the notion that Zhoukoudian III is likely a young
adult nearing the completion of growth, following
the conclusions of Mann (1981), Antón (2001b),
and Durband et al. (2002).
The results obtained for the recently described
Pithecanthropus Skull IX were also striking. This
specimen was statistically significantly distant from
the vast majority of specimens tested in each of the
four analyses. Additionally, the fossil was often
placed far from the clusters of specimens in the
distance plots. However, due to the preliminary
nature of the descriptions so far afforded this
specimen (Arif et al., 2001, 2002; Tyler and
Sartono, 2001) and the ongoing nature of its
reconstruction (Arif et al., 2002) we feel that
these results should be approached with extreme
caution.
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Kidder (1998) concluded that insufficient evidence existed for multiple species within H. erectus
sensu lato. However, this study indicates that the
Zhoukoudian cranial vaults possess metric characteristics that appear to be derived relative to the
condition present in the African and Indonesian
crania. These findings counter results from
many non-metric examinations that assert that
H. erectus cannot be subdivided (e.g. Kennedy,
1991; Bräuer and Mbua, 1992). The variation
found in the current study is not patterned geographically, however. The specimen from Hexian
does not exhibit metric characteristics that resemble
those found at Zhoukoudian. In addition, the nonmetric traits used by many authors (e.g., Andrews,
1984; Stringer, 1984; Wood, 1984) to differentiate
specimens within H. erectus do not correlate with
this craniometric variation (Durband and Kidder,
2000). Thus, there is no consistent pattern of metric
and non-metric variation that would indicate that a
multiple-species scenario is necessarily appropriate
for the fossils currently subsumed in H. erectus
sensu lato, with the possible exception of autapomorphic cranial base features of the Ngandong and
Sambungmacan fossils (Durband and Kidder,
2000; Durband, 2002a,b; Baba et al., 2003).
The differences in craniometric pattern explored
here are more likely attributable to two factors.
Clinal variation could have influenced the shape of
the skull at Zhoukoudian through adaptation to a
colder climate (e.g. Etler, 1994). Work by Beals
(1972; Beals et al., 1983) shows a correlation
between skull shape and climate and indicates a
trend towards brachycephaly in colder areas. Data
provided for H. erectus supports this conclusion
(Beals et al., 1983). Wolpoff (1999: 499) suggested
that the Chinese assemblage provides evidence for a
“gradient in morphology running from the north to
the south of East Asia.” Antón (2002) is also
inclined to accept this view. This morphological
gradient could be due, at least in part, to these
climatically induced changes in skull shape. Genetic
drift might also explain the differences in craniometric pattern. Currently the variant skull form is
limited to northern China at Zhoukoudian, and it
may also be present at Nanjing (Antón, 2002).
Because of the more fragmentary condition of the
Nanjing fossils we were unable to include them in
313
this analysis, but they are said to resemble the
Zhoukoudian crania (Etler, 1996; Wolpoff, 1999).
Due to its location on the edge of the known
geographic range of H. erectus, limited opportunities for gene flow would have been available in
northern China. This relative isolation could have
contributed substantially to the manifestation of
this new craniometric pattern. Thorne (1980:36) has
noted that such isolation may lead to “pronounced
divergences in the characteristics of different geographically peripheral populations, especially if
these are distinguished environmentally.”
Conclusion
The results of this project indicate that the
Zhoukoudian hominids are characterized by a
cranial vault shape unlike that seen in other representatives of Homo erectus. Each of the four
multivariate analyses performed indicates that a
pattern of statistically significant distances separates the Zhoukoudian specimens from other
African and Indonesian fossils as well as the
Hexian calvaria. The Zhoukoudian hominids are
characterized by a wide midvault and relatively
narrow frontal and occipital bones, while the
African and Indonesian hominids and the Hexian
specimen have similarly broad frontal, midvault,
and occipital dimensions. This separation between
Zhoukoudian and the other crania sampled is
unlikely to be the result of sexual dimorphism or
temporal variation, as the Chinese fossils are intermediate in age and it is probable that both sexes
are represented in that sample. It is more likely
that this variation is caused by either adaptation to
a colder environment or genetic drift. These results
do not suggest that a multiple-species scenario is
necessary to encompass the variation present in the
sample. However, further examination is needed in
order to understand the complex morphologies
currently subsumed in H. erectus.
Acknowledgements
The authors would like to thank Richard Jantz
for use of his DISPOP computer program for
314
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
this analysis as well as his considerable help and
patience with our many questions. Fachroel Aziz
graciously provided an unpublished biauricular
breadth measurement for the Sambungmacan 4
specimen. Bill Kimbel and two anonymous reviewers provided helpful comments that improved
the paper.
References
Andrews, P., 1984. An alternative interpretation of the characters used to define Homo erectus. Cour. Forsch.-Inst.
Senckenberg 69, 167–175.
Antón, S.C., 2001a. Cranial evolution in Asian Homo erectus:
the Ngandong hominids. Geological Research Development
Centre Special Publication No. 27, 39–46.
Antón, S.C., 2001b. Cranial growth in Homo erectus. In:
Minugh-Purvis, N., McNamara, K.J. (Eds.), Human
Evolution Through Developmental Change. Johns Hopkins
University Press, Baltimore, pp. 349–380.
Antón, S.C., 2002. Evolutionary significance of cranial variation in Asian Homo erectus. Am. J. Phys. Anthrop. 118,
301–323.
Antón, S.C., Marquez, S., Mowbray, K., 2002. Sambungmacan
3 and cranial variation in Asian Homo erectus. J. Hum.
Evol. 43, 555–562.
Arif, J., Baba, H., Suparka, M.E., Zaim, Y., Setoguchi, T.,
2001. Preliminary study of Homo erectus skull IX
(Tjg-1993.05) from Sangiran, Central Java, Indonesia. Bull.
Natn. Sci. Mus., Tokyo Series D 27, 1–17.
Arif, J., Kaifu, Y., Baba, H., Suparka, M.E., Zaim, Y.,
Setoguchi, T., 2002. Preliminary observation of a new
cranium of Homo erectus (Tjg-1993.05) from Sangiran,
central Java. Anthrop. Sci. 110, 165–177.
Baba, H., Aziz, F., Kaifu, Y., Suwa, G., Kono, R.T., Jacob, T.,
2003. Homo erectus calvarium from the Pleistocene of Java.
Science 299, 1384–1388.
Beals, K.L., 1972. Head form and climatic stress. Am. J. Phys.
Anthrop. 37, 85–92.
Beals, K.L., Smith, C.L., Dodd, S.M., 1983. Climate and the
evolution of brachycephalization. Am. J. Phys. Anthrop.
62, 425–437.
Black, D., 1929. Preliminary notice of the discovery of an adult
Sinanthropus skull at Chou Kou Tien. Bulletin of the
Geological Society of China 8, 15–32.
Black, D., 1930. On an adolescent skull of Sinanthropus
pekinensis in comparison with an adult skull of the same
species and with other hominid skulls, recent and fossil.
Palaeontol. Sin. Ser. D 7, 1–144.
Bräuer, G., Mbua, E., 1992. Homo erectus features used in
cladistics and their variability in Asian and African
hominids. J. Hum. Evol. 22, 79–108.
Corruccini, R.S., 1992. Metric reconsideration of the Skhul IV
and IX and Border Cave I crania in the context of modern
human origins. Am. J. Phys. Anthrop. 87, 433–445.
Darroch, J.H., Mosimann, J.E., 1985. Canonical and principal
components of shape. Biometrika 72, 241–252.
Defrise-Gussenhoven, E., 1967. Generalized distance in
genetic studies. Acta Genet. Med. Gemellol (Roma) 17,
275–288.
Delson, E., Harvati, K., Reddy, D., Marcus, L.F., Mowbray,
K., Sawyer, G.J., Jacob, T., Márquez, S., 2001. The
Sambungmacan 3 Homo erectus calvaria: a comparative
morphometric and morphological analysis. Anat. Rec. 262,
380–397.
Durband, A.C., 2002a. The squamotympanic fissure in the
Ngandong and Sambungmacan hominids: a reply to Delson
et al. Anat. Rec. 266, 138–141.
Durband, A.C., 2002b. The view from down under: a test of
the multiregional hypothesis of modern human origins
using the basicranial evidence from Australasia. Invited
paper presented at the 17th Congress of the Indo-Pacific
Prehistory Association, Taipei, Taiwan, September 9–15.
Durband, A.C., Kidder, J.H., 2000. The question of speciation
in Homo erectus revisited II: the non-metric evidence. Am.
J. Phys. Anthrop. 30(Suppl.), 144.
Durband, A.C., Kidder, J.H., Jantz, R., 2002. A multivariate
analysis of the Hexian Homo erectus calvarium. Am. J.
Phys. Anthrop. 34(Suppl.), 66.
Etler, D.A., 1994. The Chinese Hominidae: new finds, new
interpretations. Ph.D. Dissertation, University of
California, Berkeley.
Etler, D.A., 1996. The fossil evidence for human evolution in
China. A. Rev. Anthrop. 25, 275–301.
Groves, C.P., Mazák, V., 1975. An approach to the taxonomy
of the Hominidae: gracile Villafranchian hominids of
Africa. Casopis Min. Geol. 20, 225–247.
Grün, R., Huang, P.H., Wu, X., Stringer, C.B., Thorne, A.,
McCulloch, M., 1997. ESR analysis of teeth from the
palaeoanthropological site of Zhoukoudian, China. J. Hum.
Evol. 32, 83–91.
Hawks, J., Oh, S., Hunley, K., Dobson, S., Cabana, G.,
Dayalu, P., Wolpoff, M.H., 2000. An Australasian test of
the recent African origin theory using the WLH-50
calvarium. J. Hum. Evol. 39, 1–22.
Howells, W.W., 1973. Cranial variation in man: a study by
multivariate analysis of patterns of difference among recent
populations. Pap. Peabody Mus. Arch. Ethnol, Harvard
University Press, Cambridge.
Howells, W.W., 1989. Skull shapes and the map: craniometric
analyses in the dispersion of modern Homo. Pap. Peabody
Mus. Arch. Ethnol., Harvard University Press, Cambridge.
Jacob, T., Morphology and paleoecology of early man in Java.
In: Tuttle, R. (Ed.) Paleoanthropology, Morphology, and
Paleoecology. Mouton, The Hague, pp. 311–25.
Jantz, R.L., Owsley, D.W., 2001. Variation among early North
American crania. Am. J. Phys. Anthrop. 114, 146–155.
Kennedy, G.E., 1991. On the autapomorphic traits of Homo
erectus. J. Hum. Evol. 20, 375–412.
Kidder, J.H., 1998. Morphometric variability in Homo erectus.
Am. J. Phys. Anthrop. 24(Suppl.), 138.
J.H. Kidder, A.C. Durband / Journal of Human Evolution 46 (2004) 299–315
Kidder, J.H., Durband, A.C., 2000. The question of speciation
in Homo erectus revisited I: the metric evidence. Am. J.
Phys. Anthrop. 30(Suppl.), 195.
Kramer, A., 1993. Human taxonomic diversity in the
Pleistocene: does Homo erectus represent multiple hominid
species? Am. J. Phys. Anthrop. 91, 161–171.
Mann, A., 1981. The significance of the Sinanthropus casts, and
some paleodemographic notes. In: Sigmon, B.A., Cybulski,
J.S. (Eds.), Homo erectus: Papers in Honor of Davidson
Black. University of Toronto Press, Toronto, pp. 41–61.
Mosimann, J.E., James, F.C., 1979. New statistical methods for
allometry with application to Florida red-winged
blackbirds. Evolution 33, 444–459.
Rightmire, G.P., 1990. The Evolution of Homo erectus: Comparative Anatomical Studies of an Extinct Human Species.
Cambridge University Press, Cambridge.
Santa Luca, A.P., 1980. The Ngandong fossil hominids: a
comparative study of a Far Eastern Homo erectus group.
Yale Univ. Publ. Anthrop, New Haven.
Shen, G., Ku, T.-L., Cheng, H., Edwards, R.L., Yuan, Z.,
Wang, Q., 2001. High-precision U-series dating of
Locality 1 and Zhoukoudian, China. J. Hum. Evol. 41,
679–688.
Simmons, T., Falsetti, A.B., Smith, F.H., 1991. Frontal
bone morphometrics of southwest Asian Pleistocene
hominids. J. Hum. Evol. 20, 249–269.
315
Stringer, C.B., 1984. The definition of Homo erectus and the
existence of the species in African and Europe. Cour.
Forsch.-Inst. Senckenberg 69, 131–143.
Swisher III, C.C., Rink, W.J., Antón, S.C., Schwarcz, H.P.,
Curtis, G.H., Suprijo, A., Widiasmoro, 1996. Latest Homo
erectus of Java: potential contemporaneity with Homo
sapiens in Southeast Asia. Science 274, 1870–1874.
Thorne, A.G., 1980. The longest link: human evolution in
Southeast Asia and the settlement of Australia. In: Fox,
J.J., Garnaut, R., McCawley, P., Mackie, J.A.C. (Eds.),
Indonesia: Australian Perspectives. Australian National
University, Canberra, pp. 35–43.
Tyler, D.E., Sartono, S., 2001. A new Homo erectus cranium
from Sangiran, Java. Hum. Evol. 16, 13–25.
Weidenreich, F., 1943. The skull of Sinanthropus pekinensis: a
comparative study on a primitive hominid skull. Palaeontol.
Sin. New Ser. D 10, 1–298.
Wolpoff, M.H., 1999. Paleoanthropology, second ed. McGraw
Hill, Boston.
Wood, B.A., 1984. The origin of Homo erectus. Cour. Forsch.Inst. Senckenberg 69, 99–111.
Wood, B.A., 1991. Koobi Fora Research Project Vol. 4:
Hominid Cranial Remains. Clarendon Press, Oxford.
Wu, X., Poirier, F.E., 1995. Human Evolution in China: A
Metric Description of the Fossils and a Review of the Sites.
Oxford University Press, Oxford.