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Congruence of individual cranial bone morphology and neutral molecular affinity patterns in modern humans.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:205–215 (2009)
Congruence of Individual Cranial Bone Morphology and
Neutral Molecular Affinity Patterns in Modern Humans
Noreen von Cramon-Taubadel*
Department of Anthropology, University of Kent, Canterbury, CT2 7NR, UK
KEY WORDS
temporal bone; neutral evolution; geometric morphometrics; population history
ABSTRACT
Recent studies have demonstrated that
the shape of the human temporal bone is particularly
strongly correlated with neutral genetic expectation,
when compared against other cranial regions, such as the
vault, face, and basicranium. In turn, this has led to suggestions that the temporal bone is particularly reliable in
analyses of primate phylogeny and human population history. While several reasons have been suggested to explain
the temporal bone’s strong fit with neutral expectation,
the temporal bone has never systematically been compared against other individual cranial bones defined using
the same biological criteria. Therefore, it is currently
unknown whether the shapes of all cranial bones possess
reliable information regarding neutral genetic evolution,
or whether the temporal bone is unique in this respect.
This study tests the hypothesis that the human temporal
bone is more congruent with neutral expectation than six
other individual cranial bones by correlating population
affinity matrices generated using neutral genetic and 3D
craniometric data. The results demonstrate that while the
temporal bone shows the absolute strongest correlation
with neutral genetic data compared with all other bones,
it is not statistically differentiated from the sphenoid,
frontal, and parietal bones in this regard. Potential reasons for the temporal bone’s consistently strong fit with
neutral expectation, such as its overall anatomical complexity and/or its contribution to the architecture of the
basicranium, are examined. The results suggest that
future phylogenetic and taxonomic studies would benefit
from considering the shape of the entire cranium minus
those regions that deviate most from neutrality. Am J
Phys Anthropol 140:205–215, 2009. V 2009 Wiley-Liss, Inc.
In recent years, the temporal bone has been the focus
of several taxonomic and phylogenetic studies of primate
taxa (Lockwood et al., 2002, 2004, 2005; Harvati, 2003;
Harvati and Weaver, 2006a,b; Terhune et al., 2007;
Smith et al., 2007; Smith, 2009). For example, in a distance-based phylogenetic analysis of the hominoids,
Lockwood et al. (2004) employed temporal bone shape to
successfully reconstruct the Pan-Homo clade suggested
by genetic data. Subsequent analyses of temporal bone
morphology in modern human populations (Harvati and
Weaver, 2006a,b; Smith et al., 2007) have concluded that
biological distance matrices constructed using temporal
bone shape are highly correlated with neutral molecular
distances, while temporal bone size reflects environmental differences related to temperature and latitude. Harvati and Weaver (2006a,b) compared population distance
matrices generated using the morphology of the temporal bone, the cranial vault, and the face, with genetic
and climatic distance matrices. Their results suggested
that the temporal bone was tracking older evolutionary
events in human population history, while the vault was
tracking more recent events. In another recent study,
Smith (2009) compared the relative neutrality of several
regions of the human cranium, including the temporal
bone, the basicranium, the mandible, the face, and the
cranial vault. She also found that the temporal bone was
strongly correlated with neutral genetic distances in
modern humans, although not significantly more so than
the basicranium, the upper face or the entire cranium.
While the results of Smith (2009) differed slightly from
those found by Harvati and Weaver (2006a,b), they conform to a growing consensus view that human temporal
bone shape varies according to neutral evolutionary
expectation.
These studies highlight the importance of employing
individual regions of the primate cranium in analytical
assessments of taxonomic and phylogenetic efficacy.
Moreover, the results of Harvati and Weaver (2006a,b)
and Smith (2009) suggest that if temporal bone shape
provides a reliable indicator of past population history, it
is plausible that temporal bone shape may also provide a
more reliable means of reconstructing phylogenetic relationships amongst fossil hominins, for which we possess
only morphological data. However, the underlying biological rationale for why the temporal bone may be reliable
in this regard is currently poorly understood. Several
potential reasons have been put forward. For example,
Lockwood et al. (2004, p 4356) attribute the high phylogenetic efficacy of the temporal bone to its functional
and anatomical complexity stating that ‘‘the temporal
bone is a natural target for phylogenetic study. Its functional complexity should minimize the possibility that a
single behavioral shift in unrelated taxa could lead to
C 2009
V
WILEY-LISS, INC.
C
Grant sponsor: EU-funded SYNTHESYS initiative; Grant numbers: FR-TAF-1989; AT-TAF-2189. Grant sponsors: Leakey Trust;
Cambridge Gates Foundation; St. John’s College, Cambridge.
*Correspondence to: Noreen von Cramon-Taubadel, Department
of Anthropology, University of Kent, Canterbury, CT2 7NR, UK.
E-mail: n.von-cramon@kent.ac.uk
Received 25 September 2008; accepted 15 January 2009
DOI 10.1002/ajpa.21041
Published online 5 May 2009 in Wiley InterScience
(www.interscience.wiley.com).
206
N.
VON
CRAMON-TAUBADEL
TABLE 1. Modern human craniometric and genetic data sampled
Morphological
Genetic
Population
Museum (sample size)
Microsatellitesa
Classical markersa
Ibo
Western Pygmies
Zulu
San
Berber
Chinese (Han)
Japanese
Mongolians
Basque (French)
Italians
Russians
Hawikuh
Alaskan Inuit
Greenland Inuit
Australians
Total
NHM (30)
NHM, MH (21)
NHM (30)
NHM, MH, AMNH, NHMW, DC (31)
MH (30)
NHMW (30)
MH (30)
MH (30)
MH (30)
NHMW (30)
NHMW (30)
SNMNH (30)
AMNH (30)
SNMNH (30)
DC (30)
442
Yoruba
Biaka Pygmies
South African Bantu
San
Mozabite
Han Chinese
Japanese
Mongola
Basque (French)
Italians (Bergamo)
Russians
Pima
–
–
–
Yoruba/Ibo
Biaka Pygmies
Zulu
San
Algerian Berber
Han Chinese
Japanese
Mongol
French Basque
Italians
Russians
Pima
Alaskan Inuit
Greenland Inuit
Australian Aborigine
a
Microsatellite data were sourced from Rosenberg et al. (2002, 2005) and Rosenberg (2006) and the classical marker data were
taken from Cavalli-Sforza et al. (1994). NHM, Natural History Museum (London, UK); MH, Museé de l’Homme (Paris, France);
AMNH, American Museum of Natural History (NY, USA); NHMW, Das Naturhistorische Museum, Wien (Vienna, Austria); DC,
Duckworth Collection (Cambridge, UK); SNMNH, Smithsonian National Museum of Natural History (Washington, D.C., USA).
homoplastic similarity.’’ However, given that the temporal bone contributes to the overall morphology of the primate basicranium, which is generally believed to reliably
reflect genetic relationships between taxa (e.g., Olson,
1981; Lieberman et al., 1996, 2000a,b; Wood and Lieberman, 2001), this factor has also been cited as a possible
reason for the temporal bone’s reliability for phylogenetic
reconstruction (Harvati and Weaver, 2006a,b; Smith,
2009).
A third potential reason for the temporal bone’s relatively strong fit to a neutral model of evolutionary expectation is that it is the only individual bone ever to be
compared against other cranial regions (e.g., face, basicranium and vault). It is important to note that these
cranial regions are defined on the basis of different anatomical, developmental and functional criteria to those
used to delineate the temporal bone. To date, the temporal bone has never systematically been compared against
other equivalent cranial units (i.e., other individual cranial bones, such as the frontal, parietal and occipital).
Therefore, it is currently unknown whether the shapes
of all individual cranial bones possess reliable information regarding phylogenetic propinquity when analyzed
separately, or whether the temporal bone is unique in
this regard. It is, therefore, necessary to compare the
relative fit to a neutral model of expectation for the
major individual bones of the human cranium, if an
accurate inference model for fossil phylogeny reconstruction based on cranial morphology can be developed. If
the temporal bone’s phylogenetic reliability can be attributed to it being an individual bone, then we would
expect all cranial bones to reflect genetic distances
amongst human populations with the same degree of
accuracy.
This study tests the hypothesis that human temporal
bone morphology is more congruent with neutral genetic
expectation than other individual cranial bones and the
cranium as a whole. Here, as in previous studies employing a quantitative genetic framework to analyze patterns
of human craniometric variation (e.g., Roseman, 2004;
Harvati and Weaver, 2006a,b; Smith et al., 2007; Smith,
2009), a strong correlation between population affinity
matrices based on morphological and neutral genetic
American Journal of Physical Anthropology
data is taken to support a largely neutral model of evolution for that particular morphology. By correlating population affinity matrices based on different aspects of cranial morphology against the same neutral genetic affinity matrix, it is possible to rank individual cranial
regions in terms of their relative neutrality. Cranial
regions that better fit a neutral model of evolution are
also deemed more reliable in terms of reconstructing
past population history (Roseman, 2004; Harvati and
Weaver, 2006a,b). As pointed out by Roseman (2004),
population structure and history are analogous to phylogeny. Therefore, it can be assumed that morphological
regions found to reflect human population history also
hold greater potential for accurately reflecting phylogenetic relationships amongst extant and extinct primate
taxa.
MATERIALS AND METHODS
Materials
Materials for this study comprised three categories of
data: genetic allele frequencies, craniometric data in the
form of three-dimensional landmark configurations, and
climatic variables. Genetic data were taken from two
published sources. Autosomal microsatellite allele frequencies were collated from the HGDP-CEPH database
reported by Rosenberg and colleagues (Rosenberg et al.,
2002, 2005; Rosenberg, 2006) and available online at
http://rosenberglab.bioinformatics.med.umich.edu/diversity. Classical marker gene frequencies were collated
from data published by Cavalli-Sforza et al. (1994). Craniometric data were collected, by the author, in the form
of three-dimensional landmarks and semi-landmarks
from museum collections of modern human remains representing the populations for which genetic data were
available. In total, it was possible to match 15 globally
distributed populations for both genetic and craniometric
data (Table 1). Classical genetic data were available for
all 15 populations; however, microsatellite genetic data
were only available for 12 of the 15 populations (i.e.,
excluding the two Inuit and the Australian populations).
The microsatellite dataset comprised frequencies for
207
RELATIVE NEUTRALITY OF HUMAN CRANIAL BONES
9,347 microsatellite alleles from across 783 markers and
has been successfully employed in previous analyses of
this type (e.g., Roseman, 2004; Harvati and Weaver,
2006a,b; Smith, 2009). In the case of the classical
marker data, not all genetic loci or alleles were represented for each of the 15 populations of interest. Table 2
shows the final dataset of 59 allele frequencies representing 13 loci compiled from the extensive dataset published by Cavalli-Sforza et al. (1994). In the case of biallelic markers, only one allele frequency was employed to
generate population matrices.
TABLE 2. Classical marker loci (13) and alleles (59) matched
for 15 populations sampled for craniometric data
Locus
Cranial samples were chosen primarily on the basis of
their chronological, geographic, and ethnic match to the
available genetic data. All crania measured were adult,
anatomically complete and samples of 30 crania with
approximately equal numbers of males and females were
targeted. Climatic data were collated from the databases
described by New et al. (1999, 2002) and available online
(http://www.ipcc-data.org). Data for four climatic variables—temperature (8C), precipitation (mm/day), vapor
pressure (hPa), and cloud cover (%)—were collected for
each of the 15 populations. For each variable, three values (annual minimum, maximum, and mean) were estimated resulting in a total of 12 climatic variables (see
Table 3).
Allele
Locus
Allele
Methods
A
B
O
1
2
3
9
10
11
19
23
24
25
26
28
29
30
31
32
33
5
7
8
12
13
14
15
16
17
18
HLA-B
21
22
27
35
37
38
39
40
41
44
49
51
62
63
1
za;g
zaxg
K
1
M
P1
A
1
C
D
E
B
C
D
Geometric morphometrics. Landmarks were digitized
using a Microscribe 3DXTM digitizer (Immersion, San
Jose, CA) and associated software. Table 4 details the
numbers of landmarks digitized for each cranial bone
and Figure 1 shows the positions of all landmarks (see
Table 5 for anatomical descriptions). In addition to the
landmarks, five curves were traced using the stream
mode of the digitizer (one 3D co-ordinate captured every
4 mm) in order to quantify the shape of the parietal
bone in further detail (see Fig. 1). This was because the
numbers of anatomical landmarks available to describe
the parietal bone were limited and it was desirable to
keep the numbers of landmarks used to quantify each
bone approximately equal. Parietal semi-landmarks were
calculated by resampling each curve as a predetermined
number of equally spaced points using the freeware
Resample.exe (http://www.nycep.org/nmg/programs.html),
following the methodology described by McNulty (2005).
The five curves resampled comprised the form of the sagittal suture from Bregma to Lambda (5 semi-landmarks),
the coronal suture from Bregma to Sphenion (4 semilandmarks), the squamosal suture from Krotaphion to
Asterion (4 semi-landmarks), the lambdoid suture from
Asterion to Lambda (3 semi-landmarks) and a parietal
curve defined as the greatest distance across the parietal
bone from Lambda to Sphenion (6 semi-landmarks).
Intra-observer measurement error was assessed according to the partial superimposition method described by
von Cramon-Taubadel et al. (2007). Standard deviations
ABO
HLA-A
HLA-B
HP
IGHG1G3
KEL
KM
MN
P
PGD
PGM1
RH
TF
Data taken from Cavalli-Sforza et al. (1994).
TABLE 3. Climatic variables used to construct climatic distance matrices for 15 populations
miTemp mxTemp mnTemp miPrecip mxPrecip mnPrecip miVP mxVP mnVP miCloud mxCloud mnCloud
Alaskan
Australian
Basque
Berber
Chinese
Greenland
Hawikuh
Ibo
Italian
Japanese
Mongolian
Pygmy
Russian
San
Zulu
227.20
17.10
3.70
8.20
1.10
221.80
0.80
25.00
23.60
21.10
220.50
24.10
214.30
16.10
13.90
5.70
31.70
19.90
29.90
27.50
2.30
21.60
29.70
14.00
24.50
20.50
27.60
16.60
26.20
22.90
211.67
25.61
11.36
18.11
14.88
210.61
10.78
26.93
5.21
10.98
1.24
25.40
1.57
22.48
18.99
0.08
0.02
1.40
0.09
0.40
0.50
0.30
0.04
2.96
2.67
0.00
0.11
1.00
0.00
0.30
0.85
3.00
2.70
0.91
6.50
1.30
2.30
7.70
4.52
5.68
1.83
7.85
2.43
4.40
4.60
0.29
0.87
2.20
0.61
2.23
0.88
0.92
3.64
3.61
4.07
0.49
3.72
1.69
1.40
2.16
0.41
8.00
6.90
6.30
4.20
0.80
3.40
14.70
3.99
4.42
0.99
15.70
1.98
11.30
9.80
8.30
20.50
15.30
13.30
29.40
5.90
12.80
27.50
13.09
23.40
13.72
25.40
13.80
24.60
20.70
3.21
13.43
10.37
9.38
14.13
2.67
6.19
23.33
8.09
11.40
5.40
22.36
6.69
17.79
15.62
55.50
18.20
42.00
35.70
43.20
53.10
31.30
51.50
51.10
66.90
24.70
26.60
57.30
22.40
23.70
82.60
53.60
73.80
48.10
69.80
70.70
49.40
88.30
65.20
80.60
40.40
65.00
94.60
64.30
63.70
71.28
33.58
59.69
40.38
57.29
63.49
42.67
68.70
59.07
73.21
32.25
44.08
74.92
43.78
46.29
Temp, temperature (8C); Precip, precipitation (mm/day); VP, vapour pressure (hPa); Cloud, cloud cover (%); mi, minimum; mn,
mean; mx, maximum.
Data from New et al. (1999, 2002).
American Journal of Physical Anthropology
208
N.
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TABLE 4. Number of landmarks and principal component
scores employed to generate craniometric R- and D-matrices
Cranial region
Full cranium
Frontal
Occipital
Sphenoid
Temporal
Parietal
Maxilla
Zygomatic
a
No. of
landmarks
15 populations:
no. of PC scores
12 populations:
no. of PC scores
141
25
23
25
22
27a
19
13
138
35
33
43
45
27
39
23
129
36
33
43
44
27
39
23
Five landmarks and 22 semi-landmarks (see Fig. 1).
for five repeat measurements of all landmarks and semilandmarks ranged from 0.21 to 0.99 mm and were
deemed acceptable.
Each individual bone landmark configuration was subjected to Generalized Procrustes Analysis, tangent space
projection, and Principal Components Analysis (PCA) in
Morphologika 2.3.1. (O’Higgins and Jones, 2006) to generate morphometric input variables for constructing population affinity matrices. GPA eliminates variation
between individual cranial landmark configurations due
to translation, rotation and scaling using a least-squares
algorithm (Gower, 1966; Chapman, 1990). The Procrustes residuals were projected into a linear space tangent to the curved shape space and subjected to PCA.
Following Roseman and Weaver (2004), the resulting
principal component (PC) scores were used as shape variables for constructing the craniometric affinity matrices.
For each individual cranial region analyzed, the numbers of PCs required to explain at least 95% of the overall morphometric variance were employed (Table 4).
There is a positive relationship between numbers of
landmarks employed to capture a single cranial unit and
the numbers of PC scores produced by the analyses (i.e.,
larger configurations yield greater numbers of PCs).
However, the numbers of PC scores that account for 95%
of the total variance reflects both the initial size of the
landmark configuration employed as well as the general
‘‘complexity’’ of the shape captured. For example, the
frontal, occipital, sphenoid, and temporal bones are all
delineated by similar numbers of landmarks (22-25), yet
the sphenoid and temporal require approximately 10
more PC scores (43 and 45 respectively) to account for
their variability than the frontal and occipital (35 and 33
respectively). Thus, the number of PC scores employed
as morphometric input data reflects the relative shape
complexity of the different cranial units (i.e., complex
sphenoid/temporal relative to simple frontal/occipital).
Generating population matrices. Two types of biological affinity matrices (relationship and distance) describing the relationships between populations were generated
from the genetic and the craniometric data. Relationship
(R-) matrices (Harpending and Ward, 1982; Relethford
and Blangero, 1990) describe the scaled relationships
between pairs of populations, with values ranging from
11 to 21. Off-diagonal matrix elements describe the relationships between two populations relative to the average
distance between individual populations and the regional
centroid. Thus, positive values denote that two populations are more similar to each other than on average and
negative values denote populations are more distinct
than on average. Distance (D-) matrices were derived
American Journal of Physical Anthropology
Fig. 1. Anatomical location of landmarks and parietal semilandmarks digitized to quantify the shape of the entire cranium
including the shapes of seven individual cranial bones. See Table 5 for full anatomical descriptions of all landmarks.
from R-matrices using the Harpending and Jenkins
(1973) transformation and describe the absolute distances
between all pairs of populations. Given the lack of reliable
population-specific heritability estimates for individual
craniometric regions, all craniometric R- and D-matrices
209
RELATIVE NEUTRALITY OF HUMAN CRANIAL BONES
TABLE 5. Anatomical definitions of landmarks illustrated in Figure 1
Code
Landmark
al
Alare
ale
ast
Alveolare
Asterion
b
ba
Bregma
Basion
cal
cam
chi
Carotid canal (lat)
Carotid canal (med)
Cheek height (inf)
chs
Cheek height (sup)
co
cp
Coronale
C/P3
d
Dacryon
eama
Ext aud meatus (ant)
eami
Ext aud meatus (inf)
eamp
Ext aud meatus (pos)
ek
ekm
Ectoconchion
Ectomolare
epl
External palate length
fmo
Frontomalare orbitale
fmt
foa
fob
fop
fred
Frontomalare temp
Foramen ovale (ant)
Foramen magnum (lat)
Foramen ovale (pos)
FRED
ft
Frontotemporale
g
hf
Glabella
Hypoglossal foramen
ho
hol
i
Hormion
Hormion (lat)
Inion
in
Infranasion
inv
it
jfl
Incisivon
Infratemporale
Jugular (lat)
jfm
Jugular (med)
ju
Jugale
k
l
m
Krotaphion
Lambda
Metopion
mfl
mmc
Mandibular fossa (lat)
Max maxillary curve
mmd
ms
msa
Max maxillary depth
Mastoideale
Mastoideale (ant)
msp
Mastoideale (pos)
Anatomical definition
Source
The most lateral point on the nasal aperture taken perpendicular
to the nasal height
The most anterior point on the alveolus of the first molar
The point where the lambdoid, parietomastoid and occipitomastoid
sutures meet
The point where the coronal and sagittal sutures intersect
The point where the anterior margin of the foramen magnum
intersects the midsagittal plane
The most lateral point on the carotid canal
The most medial point on the carotid canal
The point on the inferior border of the zygomatic that represents
the endpoint of minimum cheek height
The point on the inferior orbital rim that represents the endpoint
of minimum cheek height
The most lateral point on the coronal suture
The most inferior external point between the maxillary canine and
the first pre-molar
The point of intersection of the frontolacrimal and
lacrimomaxillary suture
The most anterior point on the margin of the external auditory
meatus
The most inferior point on the margin of the external auditory
meatus
The most posterior point on the margin of the external auditory
meatus
The most lateral point on the orbital margin
The most lateral point on the outer surface of the alveolar margin
of the maxilla
The point on the inferior surface of the maxilla that denotes the
most posterior point of the alveolar process
The point where the zygomaticofrontal suture crosses the orbital
margin
The most lateral point on the zygomaticofrontal suture
The most anterior point on the foramen ovale
The most lateral point on the margin of the foramen magnum
The most posterior point on the foramen ovale
The point of intersection of the frontozygomatic,
zygomaticosphenoid and sphenofrontal sutures
The point on the frontal bone where the temporal line reaches its
most anteromedial position.
Most anterior point on the frontal bone
The most inferior, anterior point on the edge of the hypoglossal
canal
The point of attachment of the vomer and sphenoid bones
The most posterior point on the ala of the vomer
The point where the superior nuchal lines merge in the external
occipital protuberance
The point of intersection of the nasofrontal, nasomaxillary and
maxillofrontal sutures
The most posterior inferior point on the incisive fossa
The most medial point on the infratemporal crests
The most inferior, lateral point on the margin of the jugular
foramen
The most inferior, medial point on the margin of the jugular
foramen
The point in the notch between the temporal and frontal process of
the zygomatic bone
The most posterior extent of the sphenoparietal suture
The point where the sagittal and lambdoid sutures intersect.
The point where the frontal elevation above the chord from
Nasion-Bregma is greatest
The most lateral point on the mandibular fossa
The point in the depth of the notch between the zygomaxillary
suture and the alveolar process
The deepest point of the canine fossa
The most inferior, lateral point on the mastoid process
The anterior point of intersection of the mastoid process and the
external tympanic plate
The posterior point of intersection of the mastoid process and the
digastric groove
4
2a
1
1
1
Cranial units
EC, M
EC, M
EC, O, T, P
EC, F, P
EC, O
2a
EC, T
EC, T
EC, Z
2a
EC, Z
1
3
EC, F
EC, M
1
EC, F, M
EC, T
3
EC, T
EC, T
1
1
EC, Z
EC, M
3
EC, M
1
EC, F, Z
1
3
EC,
EC,
EC,
EC,
EC,
1
EC, F
1
EC, F
EC, O
1
1
EC
EC
EC, O
1
EC, F, M
1
5
EC, M
EC, S
EC, O, T
F, Z
S
O
S
F, S, Z
EC, O, T
1
EC, Z
1
1
1
EC, S, T, P
EC, O, P
EC, F
5a
3
EC, T
EC, M
3
1
2a
EC, M
EC, T
EC, T
2a
EC, T
American Journal of Physical Anthropology
210
N.
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TABLE 5. (Continued)
Code
Landmark
mss
Mastoideale (sup)
n
Nasion
na
nam
o
Nariale
Nasomaxillare
Opisthion
oca
ocl
ocs
Occipitocondyle (ant)
Occipitocondyle (lat)
Occipital subtense
ol
Orale
on
Ophryon
op
Opisthocranion
or
ors
pad
pal
pas
Orbitale
Orbitale (sup)
Palatomaxillare
Palatomaxillare (lat)
Parietal subtense
pet
Petrosal
po
Porion
pr
Prosthion
ra
spem
Radiculare
Sphenomaxillare (sup)
sphba
sphbal
Sphenobasion
Sphenobasion (lat)
sphn
ss
Sphenion
Subspinale
ssq
Sphenosquamosal
st
Stephanion
ste
sty
szp
zti
zm
Stenion
Styloid foramen
Sphenozygomatic (pos)
Zygotemporale (inf)
Zygomaxillare
zo
Zygoorbitale
zt
zts
Zygomatic tuberosity
Zygotemporale (sup)
Anatomical definition
The most superior, lateral point on the mastoid process (on the
FH)
The point of intersection of the nasofrontal suture and the
midsagittal plane.
The most inferior point on the lower rim of the nasal aperture
The most inferior point on the nasomaxillary suture
The point where the posterior margin of the foramen magnum
intersects the midsagittal plane
The most anterior, inferior point on the occipital condyle
The most lateral, inferior point on the occipital condyle
The point where the occipital elevation above the chord from
Lambda-Opisthion is greatest
The point of intersection on the palate with a line tangent to the
posterior margins of the central incisor alveoli
The point where a line drawn through both frontotemporale
crosses the midsagittal plane
The most posterior midline point, which lies at the farthest chord
length from Glabella
The most inferior midpoint on the orbital margin
The most superior midpoint of the orbital margin
The point of intersection of the palatine and the maxillary bones
The most lateral point on the palatomaxillary suture
The where the sagittal elevation above the chord from BregmaLambda is greatest
The most anterior point of the petrous element of the temporal
bone
The most superior point on the margin of the external auditory
meatus
The most anterior point on the maxillary alveolar process between
the two central incisors
The point of maximum inflection of the zygomatic processes
The most superior, lateral point of contact between the maxilla and
the lateral pterygoid plate of the sphenoid
The midline point on the sphenooccipital suture
The most lateral, inferior point on the sphenooccipital
synchondrosis
The most anterior extent of the sphenoparietal suture
The point at which the inferior edge of the nasal spine becomes
the anterior edge of the maxilla
The point of intersection of the infratemporal crest and
sphenosquamosal suture
The point where the coronal suture crosses the (inferior) temporal
line
The most medial point on the sphenosquamosal sutures
The most anterior, inferior point on the styloid foramen
The most posterior, inferior point on the sphenozygomatic suture
The most inferior point on the zygomaticotemporal suture
The most inferior, anterior point on the zygomaticomaxillary
suture
The point where the zygomaticomaxillary suture intersects with
the inferior orbital margin
The most lateral, anteriorly projecting point on the zygomatic bone
The most superior point on the zygomaticotemporal suture
Source
Cranial units
2a
EC, T
1
EC, F
2,a 6
3
1
EC, M
EC, M
EC, O
2
a
EC, O
EC, O
EC, O
1
EC, M
1
EC, F
1
EC, O
1
3
3
2a
EC,
EC,
EC,
EC,
EC
5a
EC, S, T
Z
F
M
M
1
EC, T
1
EC, M
1
EC, T
EC, S
1
3
EC, O, S
EC, O, S
1
1
EC, F, S, P
EC, M
5
EC, S, T
1
EC, F
1
EC,
EC,
EC,
EC,
EC,
2a
1
S, T
T
S
T, Z
M, Z
2
EC, M, Z
3
EC, Z
EC, T, Z
1. Martin and Saller (1957), 2. Howells (1973), 3. Lahr (1992), 4. Bass (1995), 5. Lockwood et al. (2004), 6. Grine et al. (2007).
a
Adapted from original source.
FH, Frankfurt horizon; EC, entire cranium; F, frontal; O, occipital; S, sphenoid; T, temporal; P, parietal; M, maxilla; Z, zygomatic.
were generated under the assumption of complete heritability (h2 5 1) and were therefore, by definition, minimum estimates of genetic distances.
Genetic R- and D-matrices were generated from the allele frequency data in the software RMAT 1.2, kindly
made available by John Relethford, following the model
described by Harpending and Ward (1982). Craniometric
R- and D-matrices were generated from the morphometric PC data using the software RMET 5.0, also available
American Journal of Physical Anthropology
from John Relethford, following the model described by
Relethford and Blangero (1990). The Relethford–Blangero (Relethford and Blangero, 1990) estimator of population genetic affinities based on quantitative traits is
derived from the Harpending and Ward (1982) model
and assumes an equal and additive model of inheritance
for the quantitative traits. Multivariate covariance matrices are calculated under the assumption that population phenotypic variances are proportional to genetic
211
RELATIVE NEUTRALITY OF HUMAN CRANIAL BONES
variances. For paired cranial bones (i.e., parietal, maxilla and zygomatic) only data from the right side were
employed to generate craniometric R- and D-matrices.
In addition to the craniometric and genetic affinity
matrices, population climatic distance matrices were constructed in PAST 1.7 (Hammer et al., 2001) using the 12
climatic variables shown in Table 3. These 12 variables
reflect the annual mean, maximum and minimum values
for temperature, precipitation, cloud cover, and vapor
pressure. Distance matrices were constructed by calculating the squared Euclidean distances between all pairs
of populations for all 12 variables combined. In the case
of the climatic and craniometric data, matrices were constructed twice; once for all 15 populations, and once for
the 12 populations for which microsatellite genetic data
were available. Genetic matrices were constructed for all
15 populations using the classical gene frequency data
and for the subset of 12 populations using the microsatellite allele frequency data.
Comparing population matrices. Given that matrices
violate certain statistical assumptions of traditional association tests (e.g., Pearson correlation), all matrices
(genetic, craniometric and climatic) were correlated
using Mantel matrix tests (Mantel, 1967). Here, P values
are assigned through a randomization test, where the
observed correlation between two or more matrices is
assessed against a distribution of correlations obtained
by random permutation of the rows and columns of the
matrices (Smouse and Long, 1992). The basic Mantel
test allows for the comparison of two matrices (X and Y).
Partial Mantel tests (Smouse et al., 1986) can be used to
test the strength of correlation of two matrices (X and
Y), while control for a third matrix (Z). This is achieved
by regressing the elements of X and Y onto Z, and using
the residuals from the regressions as the input for a
standard Mantel test. Full and partial Mantel tests were
performed in PASSaGE 1.1 (http://www.passagesoftware.
net). Matrix permutations were performed 10,000 times
and the critical alpha level for full Mantel comparisons
was set at a 5 0.05. Following Roseman (2004), Bonferroni correction was applied to partial Mantel tests (i.e., a
5 0.017).
In addition to the full and partial Mantel tests, a
Dow–Cheverud test (Dow and Cheverud, 1985) was performed to determine whether any two cranial regions
differed significantly in their congruence with the
genetic data. This test was employed to establish
whether the correlations of any two individual bones (A
and B) with a single genetic matrix (C) were significantly different. Here the null hypothesis is that the correlation of A and C equals the correlation of B and C.
The Dow–Cheverud test has been shown, on the basis of
simulation analyzes (e.g., Oden, 1992; Konigsberg, 1997),
to be vulnerable to spuriously high rejection rates when
the data matrices are spatially or temporally autocorrelated. Therefore, these factors will be taken into consideration when interpreting the results of this test. Dow–
Cheverud tests were performed in R, employing a code
written by the lab of C.C. Roseman.
Three separate analyses were undertaken. First, the
strength of association between the genetic and craniometric data describing each individual bone was tested
by performing Mantel matrix correlations between the
genetic R-matrices and each craniometric R-matrix.
Thereafter, a Dow–Cheverud test was performed in order
to determine whether the individual bones differed sig-
TABLE 6. Results of Mantel test correlations (r values with P
values in parentheses) of craniometric R-matrices against genetic
R-matrices
15 populations
(classical markers)
Temporal
Full cranium
Sphenoid
Parietal
Frontal
Maxilla
Occipital
Zygomatic
0.69
0.64
0.62
0.60
0.57
0.56
0.54
0.37
12 populations
(microsatellites)
(0.006)
(0.002)
(0.002)
(0.008)
(0.006)
(0.004)
(0.004)
(0.020)
0.88
0.85
0.85
0.77
0.82
0.78
0.75
0.69
(0.002)
(0.003)
(0.002)
(0.010)
(0.005)
(0.007)
(0.004)
(0.006)
nificantly in their correlations with the genetic R-matrices. Thirdly, in order to test whether any residual nonneutral variation in the craniometric data could be
explained by climatically driven adaptation, craniometric
D-matrices were correlated against climatic distance
matrices. Full Mantel matrix correlations of craniometric
and climatic distance matrices were performed to test
the extent to which human cranial bone morphology
might be influenced by climatic variation. Thereafter,
partial Mantel correlations (Smouse et al., 1986) of climatic and craniometric distance matrices, controlling for
genetic D-matrices, were conducted. These were performed to mitigate the potentially confounding effect of
shared ancestry when correlating phenotypic and environmental population affinity matrices (Strauss and
Orans, 1975; Gilligan and Bulbeck, 2007). Also known as
‘‘Galton’s dilemma,’’ true instances of climatically driven
adaptation among human populations can only be identified once shared ancestry is ruled out as the primary
cause of morphological similarity between populations
that share a climatic zone.
RESULTS
Comparison of genetic and
craniometric R-matrices
Table 6 presents the results for the comparison of the
genetic and craniometric R-matrices. All eight craniometric R-matrices (seven bones and the entire cranium)
were statistically significantly (P 0.05) correlated with
the genetic R-matrices. However, the temporal bone was
consistently the most strongly correlated with the
genetic data compared with the other six individual
bones and the entire cranium. The sphenoid bone and
the entire cranium were also relatively strongly correlated with the genetic data, while the occipital and the
zygomatic bones were consistently found to be the least
strongly correlated with the genetic data.
Dow–Cheverud test
Table 7 presents the results of the Dow–Cheverud
(DC) test, which determined whether any of the Mantel
correlations between craniometric and genetic R-matrices differed significantly from each other. In the comparison of craniometric and classical marker data (Table 7;
lower triangle), the temporal bone and entire cranium
were significantly more strongly correlated with the
genetic data than the maxilla, occipital and zygomatic
bones, while the sphenoid was more strongly correlated
with the genetic data than the occipital and the zygomatic. All other bones (parietal, frontal, maxilla and
American Journal of Physical Anthropology
212
N.
VON
CRAMON-TAUBADEL
TABLE 7. Results of Dow–Cheverud tests (p1Z with P values in parentheses) of correlations between craniometric and
genetic R-matrices
Temporal
Temporal
Full cranium
Sphenoid
Parietal
Frontal
Maxilla
Occipital
Zygomatic
0.09
20.12
20.15
20.16
20.19
20.27
20.41
(0.176)
(0.117)
(0.086)
(0.052)
(0.044)
(0.005)
(0.002)
Full cranium
Sphenoid
20.07 (0.262) 20.06
0.002
20.03 (0.368)
20.06 (0.295) 20.04
20.14 (0.082) 20.08
20.18 (0.029) 20.11
20.16 (0.050) 20.14
20.38 (0.001) 20.33
Parietal
(0.311) 20.20 (0.055)
(0.468) 20.12 (0.154)
20.12 (0.143)
(0.370)
(0.240)
0.03 (0.399)
(0.135) 20.05 (0.330)
(0.050) 20.09 (0.166)
(0.004) 20.25 (0.011)
Frontal
20.11
20.07
20.06
20.06
(0.177)
(0.305)
(0.294)
(0.280)
20.04 (0.330)
20.06 (0.250)
20.25 (0.012)
Maxilla
20.14
20.11
20.09
20.01
20.05
(0.138)
(0.154)
(0.197)
(0.452)
(0.342)
Occipital
20.25
20.21
20.15
20.02
20.09
20.04
(0.030)
(0.045)
(0.106)
(0.434)
(0.218)
(0.393)
0.02 (0.408)
0.24 (0.013) 20.19 (0.026)
Zygomatic
20.26
20.27
20.21
20.09
20.18
20.13
20.09
(0.024)
(0.025)
(0.054)
(0.236)
(0.064)
(0.166)
(0.249)
Lower triangle, comparisons of 15-population matrices; upper triangle, comparisons of 12-population matrices. Significantly different results are in boldface.
TABLE 8. Results of Mantel test correlations (r values with P values in parentheses) of craniometric and climatic distance matrices
15 populations
Full
Full cranium
Sphenoid
Frontal
Maxilla
Temporal
Parietal
Occipital
Zygomatic
0.39
0.39
0.37
0.37
0.30
0.28
0.24
0.17
(0.002)
(0.003)
(0.004)
(0.002)
(0.014)
(0.014)
(0.018)
(0.070)
12 populations
Partiala
0.26
0.26
0.24
0.28
0.14
0.17
0.17
0.10
(0.040)
(0.020)
(0.030)
(0.015)
(0.250)
(0.170)
(0.120)
(0.440)
Full
0.01
0.23
0.04
0.14
0.15
0.22
0.19
0.01
(0.450)
(0.070)
(0.370)
(0.140)
(0.200)
(0.240)
(0.140)
(0.430)
Partiala
0.07
0.32
0.13
0.20
0.22
0.32
0.24
0.04
(0.710)
(0.030)
(0.440)
(0.150)
(0.190)
(0.050)
(0.090)
(0.730)
a
Partial Mantel tests are correlations of climatic and craniometric distances, controlling for genetic distances. Significant correlations are in boldface.
occipital) showed significantly higher correlations with
the genetic data than the zygomatic. In the comparison
of craniometric and microsatellite data (Table 7; upper
triangle), the temporal bone and the entire cranium
showed significantly higher correlations with the genetic
data than both the occipital and zygomatic. These
results indicate that bones vary statistically in terms of
their congruence with neutral genetic data and that the
temporal bone’s relatively strong congruence with neutral expectation cannot simply be ascribed to it being an
individual bone. However, the results suggest a clear distinction in terms of genetic congruence between two
groups of bones. While the temporal, sphenoid, frontal,
and parietal bones are generally all equally strongly correlated with genetics, the occipital, zygomatic and (to a
lesser extent) the maxilla are all less congruent with
neutral expectation. Given that the eight craniometric
R-matrices tested are likely to be spatially autocorrelated (e.g., Relethford, 2004), this conclusion based on
the DC test should be treated with some caution (Oden,
1992). The general conclusion that the temporal bone is
not unique amongst cranial bones, in terms of its
strength of association with neutral genetic data, holds
true as the presence of data autocorrelation is likely to
increase rejection rates of the null hypothesis that all
cranial regions are equally strongly correlated with the
genetic data. Therefore, if anything, this test has underestimated the numbers of bones which are as strongly
correlated with the molecular data as the temporal bone.
Comparison of climatic and craniometric
D-matrices
Table 8 presents the results of all craniometric and climatic comparisons performed. Mantel matrix correlations of climatic and craniometric D-matrices for all 15
populations (including the Inuit and Australian populaAmerican Journal of Physical Anthropology
tions) found that all cranial units, except for the zygomatic bone, were significantly correlated with climate.
However, the strength of these correlations (r values)
was substantially lower than for the comparison of
genetic and craniometric R-matrices. For the comparison
of the 12-population subset (excluding the Inuit and Australian populations), no cranial unit was found to correlate significantly with climate. Partial correlations of climatic and craniometric D-matrices, controlling for
genetic D-matrices found that only the maxilla was significantly correlated with climate following Bonferroni correction (a 5 0.017), when all 15 populations were included. No cranial units were correlated with climate in
the 12-population comparison. These results mirror those
of previous studies (e.g., Harvati and Weaver, 2006b),
which found that removal of high-latitude Inuit populations from the analysis resulted in a non-significant correlation between craniometric and climatic distances. Moreover, once genetic distance has been accounted for, it
appears that only the maxilla bone is significantly (but
weakly) correlated with climate, suggesting that climatic
variation cannot explain the overall patterns of non-neutral craniometric diversity observed in this sample of
globally distributed human populations.
DISCUSSION
The results of these analyses suggest that the temporal bone’s relatively strong fit with neutral expectation
in modern humans cannot be attributed entirely to it
being an individual bone. This is because other individual cranial bones, such as the zygomatic and the occipital, were found to be statistically less strongly correlated
with neutral expectation than the temporal bone.
Although the results show that the temporal bone was
consistently the most strongly correlated (highest overall
r values) with the genetic data when compared with six
RELATIVE NEUTRALITY OF HUMAN CRANIAL BONES
other cranial bones, the results of the Dow–Cheverud
test suggest that the sphenoid, frontal and parietal
bones cannot be differentiated statistically from the temporal bone in terms of their congruence with genetic
data. This would imply that these three bones should
also be taken into stronger consideration in future analyses of congruence between craniometric and neutral
genetic variation. It is also notable that the frontal, parietal, greater wings of the sphenoid, and the squamous
portion of the temporal bone form the majority of the
cranial vault, the shape of which Harvati and Weaver
(2006a,b) found to reliably reflect neutral patterns of
variation in modern humans (although see Roseman,
2004; Smith, 2009).
What light can these results shed on the alternative
reasons that have been put forward for the temporal
bone’s congruence with neutral genetic data? It has been
suggested (Harvati and Weaver, 2006a,b; Smith, 2009)
that the temporal bone’s contribution to the overall
architecture of the basicranium may explain its genetic
congruence. This is because the endochondrally ossifying
basicranium is thought to be under strong genetic control and is, therefore, relatively unaffected by epigenetic
sources of variation (Lieberman et al., 1996, 2000a,b;
Wood and Lieberman, 2001). The results of this study do
not support the ‘‘basicranial’’ explanation for the temporal bone’s genetic congruence, as the correlations of
other non-basicranial bones (i.e., the frontal and parietal) with neutral genetic data were not significantly different. Moreover, a large portion of the occipital bone
contributes to the overall architecture of the basicranium, yet the occipital bone was consistently one of the
least strongly correlated with genetic data.
Lockwood et al. (2004) proposed that the temporal
bone’s phylogenetic efficacy might be linked with its anatomical/functional complexity and hence, its relative immunity from sources of homoplasy. This study found
some support for this notion in that another complex
bone, the sphenoid, was consistently found to be the second most genetically congruent after the temporal bone.
The sphenoid and temporal bones share some biological
characteristics: they are both compound in terms of their
patterns of developmental ossification (i.e., endochondral
and intramembranous regions), they contribute architecturally to both the basicranium and the cranial vault,
and are (arguably) amongst the most anatomically complex within the primate cranium. However, the relatively
anatomically simple frontal and parietal bones were also
found to correlate strongly with genetic data, suggesting
that anatomical and functional complexity cannot fully
explain the temporal bone’s phylogenetic efficacy. Indeed
the biological criterion of ‘‘complexity’’ is difficult to evaluate in terms of its reliability for predicting phylogenetic
efficacy. For instance, Perez et al. (2007: p. 30) employ
the same reasoning to suggest that the facial skeleton
may be relatively immune to homoplasy stating that
because the ‘‘facial skeleton is related to brain development, mastication, and the respiratory and other functional systems. . . . Its functional complexity minimizes
the possibility that a single behavioural shift in unrelated taxa could lead to homoplastic similarity across a
suite of features.’’ Yet, it has been demonstrated that in
comparison with other cranial regions, facial shape is a
relatively poor indicator of past population history
(Roseman, 2004; Harvati and Weaver, 2006a,b; Smith,
2009), highlighting the ambiguity surrounding the biological criterion of ‘‘complexity.’’
213
In order to identify and better understand the biological underpinnings for why some cranial regions reflect
neutral evolutionary processes more reliably than others,
it is worth acknowledging that many studies have shown
the entire cranium to generally be a reliable indicator of
neutral expectation (Relethford, 1994, 2001, 2004; González-José et al., 2004; Roseman, 2004; Roseman and
Weaver, 2004; Harvati and Weaver, 2006b; Smith, 2009).
This finding was confirmed here, with the entire cranium found to be at least as strongly correlated with
genetic data as the temporal, sphenoid, frontal and parietal bones. Therefore, it may be more appropriate to
characterize those regions of the primate cranium that
should be excluded from future analyses of phylogeny
and taxonomy, rather than preferentially targeting single individual cranial regions for inclusion. Hence, on
the basis of the results generated here, it might be suggested that future analyses quantify the entire cranium,
minus the occipital and the facial bones (maxilla and zygomatic). In addition, it is easier to identify commonalities amongst these three relatively ‘‘non-neutral’’ bones:
they all possess sites of major muscle attachment (e.g.,
masticatory or nuchal) and are, therefore, more prone to
the potentially non-neutral influences of biomechanical
stress. The results of the comparison of climatic and craniometric distances showed that climatic factors could
not explain the divergence from neutrality for these
three bones. It is interesting to note, however, that the
maxilla was the only bone found to correlate significantly with climatic variation following correction for
genetic distance. This supports the suggestion made by
Roseman (2004), Roseman and Weaver (2004), and Harvati and Weaver (2006a,b) that some aspects of facial
shape variation in humans may be linked to climatically
driven adaptation.
CONCLUSIONS
The results of this study confirm that human temporal
bone shape is a reliable indicator of past population history. However, by comparing the temporal bone with six
other individual cranial bones, the results demonstrate
that the temporal bone is not unique in this regard since
it cannot be distinguished statistically from the frontal,
parietal or sphenoid bones in terms of its congruence
with neutral genetic data. Various hypotheses have been
put forward to explain the temporal bone’s general phylogenetic efficacy and were examined in the light of the
results obtained here. The temporal bone’s phylogenetic
efficacy cannot be explained on the basis of its anatomical/functional complexity, nor on the basis of its inclusion
in the basicranium. While other, as yet unknown, biological rationale may underpin the relative neutrality of
temporal bone morphology, the results of this study
would suggest that future analyses would benefit from
quantification of the entire cranial shape and exclude
only those regions found to deviate most from neutrality
(i.e., the zygomatic and occipital bones). Future studies
into the congruence of individual regions of the primate
cranium with molecular affinity patterns will shed further light on the extent to which primate cranial morphology has been shaped by neutral and selective evolutionary forces. These data will become crucial for building an accurate inference model for the morphological
evolution of fossil hominins.
American Journal of Physical Anthropology
214
N.
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CRAMON-TAUBADEL
ACKNOWLEDGMENTS
I am indebted to John Relethford for kindly making
available his RMET and RMAT software, and to Charles
Roseman and Mark Grabowski for kindly providing their
R code for the Dow–Cheverud test. For their hospitality
during data collection, I wish to thank Ian Tattersall
and Gary Sawyer of the AMNH, Dave Hunt of the
Smithsonian NMNH, Phillip Mennecier of the Museé de
l’Homme, Robert Kruszynski of the NHM, Maria Teschler-Nicola of the Naturhistorishe Museum, Vienna, and
Silvia Kirchengast at the University of Vienna. For discussion and assistance relating to this research, I wish
to thank Leslie Aiello, Karen Baab, Brenda Frazier, Toomas Kivisild, Marta Lahr, Stephen Lycett, Paul
O’Higgins, and Lucio Vinicius. I am additionally grateful
to M.M. Lahr for the loan of a Microscribe digitizer. I
thank Christopher Ruff, an associate editor, and two
anonymous reviewers for helpful and constructive comments, which much improved this manuscript.
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