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An interspecific analysis of relative jaw-joint height in primates.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:519–530 (2010)
An Interspecific Analysis of Relative Jaw-Joint Height
in Primates
Brooke A. Armfield1,2* and Christopher J. Vinyard1,2
1
Department of Anatomy and Neurobiology, Northeastern Ohio Universities College of Medicine (NEOUCOM),
Rootstown, OH 44272
2
Skeletal Biology Research Focus Area, NEOUCOM, Rootstown, OH 44272
KEY WORDS
posterior facial height; basicranial flexion; facial kyphosis; craniofacial growth
ABSTRACT
Jaw-joint height (JJH) above the occlusal plane is thought to be influenced by cranial base
angle (CBA) and facial angulation during growth. To better understand how JJH relates to midline craniofacial
form, we test the hypothesis that relative increases in
JJH are correlated with increasing CBA flexion and
facial kyphosis (i.e., ventral bending) across primates.
We compared JJH above the occlusal plane to CBA and
the angle of facial kyphosis (AFK) across adults from 82
species. JJH scales with positive allometry relative to a
skull geometric mean in anthropoids and most likely
strepsirrhines. Anthropoid regressions for JJH are elevated above strepsirrhines, whereas catarrhines exhibit
a higher slope than platyrrhines. Semipartial correlations between relative JJH and both CBA and AFK
show no association across a small strepsirrhine sample,
limited associations among catarrhines and anthropoids,
but strong correlations in platyrrhines. Contrary to our
hypothesis, however, increases in relative JJH are correlated with relatively less flexed basicrania and more airorhynch faces (i.e., reduced ventral bending) in platyrrhines. The mosaic pattern of relationships involving
JJH across primate clades points to multiple influences
on JJH across primates. In clades showing little association with basicranial and facial angles, such as strepsirrhines, the potential morphological independence of JJH
may facilitate a relative freedom for evolutionary
changes related to masticatory function. Finally, failure
to associate relative JJH and basicranial flexion in most
clades suggests that the relatively taller JJH and more
flexed basicrania of anthropoids compared to strepsirrhines may have evolved as an isolated event during the
origin of anthropoids. Am J Phys Anthropol 142:519–
530, 2010. V 2010 Wiley-Liss, Inc.
The height of the jaw joint above the occlusal plane
(JJH) is hypothesized to be functionally and/or developmentally integrated with other craniofacial regions
including components of both the neurocranium and facial skull. These hypotheses center on two concepts: (1)
there is a functional component to selection for taller
JJH enhancing masticatory performance and/or (2) there
is a growth relationship between the cranial base and
face that influences the height of the jaw joint. Functional hypotheses concentrate on the implications of JJH
for masticatory mechanics related to maximum jaw
opening and/or bite force (e.g., Biegert, 1963; Zingeser,
1973; Greaves, 1974, 1980, 1995; Herring and Herring,
1974; Ward and Molnar, 1980; Osborn, 1987; Ravosa
et al., 2000; Williams et al., 2002; Vinyard et al., 2003).
Alternatively, growth- and development-related hypotheses focus on how posterior facial height is influenced by
changes in basicranial and/or upper facial morphology
(e.g., Enlow and Hunter, 1968; McCollum, 1997, 1999;
McCarthy, 2001; Sondang et al., 2003; Bastir and Rosas,
2004, 2005, 2006). For example, the relatively taller JJH
of living anthropoids compared to strepsirrhines has
been explained by Ravosa et al. (2000) as related to
increased flexion of the anthropoid cranial base and concomitant changes in facial kyphosis.
Although growth-related influences on posterior facial
height have been studied in humans and other apes
(Enlow and Hunter, 1968; Enlow, 1990; Bastir and
Rosas, 2004, 2005, 2006), we lack a primate-wide analysis of associations between JJH, cranial base angulation
(CBA), and angle of facial kyphosis (AFK). By exploring
these relationships across primate clades, we hope to
better understand how evolutionary changes in cranial
base and facial regions might influence JJH variation
across primates [see Lieberman et al. (2000)]. These
results may also help identify instances where changes
in craniofacial form that are unrelated to the masticatory apparatus have an effect on masticatory function
(Ravosa et al., 2000; Bastir and Rosas, 2005).
C 2010
V
WILEY-LISS, INC.
C
Cranial base and facial growth-related
influences on JJH
The growth and form of the cranial base, particularly,
the angle formed between anterior and posterior basicranial segments, is argued to play an important role in
determining primate skull form (e.g., Lieberman et al.,
2000 and references therein). Increasing relative brain
size across primates, is widely hypothesized to result in
Grant sponsors: Sigma-Xi, Boise Fund, AMNH, NSF; Grant numbers: SBR-9701425, BCS-0094666; Grant sponsor: L.S.B. Leakey
Foundation.
*Correspondence to: Brooke A. Armfield, Department of Anatomy
and Neurobiology—NEOUCOM, 4209 St. Rt. 44, Box 95, Rootstown,
OH 44272. E-mail: bgarner@neoucom.edu
Received 24 May 2009; accepted 10 November 2009
DOI 10.1002/ajpa.21251
Published online 1 February 2010 in Wiley InterScience
(www.interscience.wiley.com).
520
B.A. ARMFIELD AND C.J. VINYARD
Fig. 1. Diagram depicting a general hypothesized set of relationships among craniofacial elements examined here (see text for
more details). In anthropoids, increases in brain size relative to basicranial length are hypothesized to cause increased basicranial
flexion (1). A more flexed cranial base angle is hypothesized to influence orbital orientation, facial kyphosis (2), and posterior facial
height (i.e., jaw-joint height, JJH) (3). Increased facial kyphosis may also correlate with increased JJH (4). Finally, changes in JJH
have functional consequences for masticatory apparatus performance related to biting, chewing, and jaw-opening (5). Additional
linkages (including bi-directional linkages) have been suggested, but are omitted for simplicity.
a more flexed cranial base to accommodate an enlarged
brain (Moss, 1958; DuBrul and Laskins, 1961; Biegert,
1963; Vogel, 1968; Ross and Ravosa, 1993; Ross and
Henneberg, 1995; Ross, 1996; Spoor, 1997; Lieberman et
al., 2000; Ross et al., 2004) (Fig. 1). Tests of this spatial
packing hypothesis yield significant association between
relative adult brain size and CBA across several primate
clades (e.g., Ross and Ravosa, 1993; Ross et al., 2004).1
Additionally, the morphology of the cranial base is
hypothesized to influence upper and mid-facial form
(Dabelow, 1929, 1931; Enlow and Hunter, 1968; Enlow
and McNamara, 1973; Enlow, 1990; Ross and Ravosa,
1993; Spoor, 1997; Lieberman et al., 2000, 2008; Ravosa
et al., 2000; McCarthy and Lieberman, 2001; Bastir and
Rosas, 2004, 2005, 2006; Bastir et al., 2004; Kuroe et al.,
2004).2 Basic support for this observation follows from
the facts that (1) basicranial growth largely precedes
facial growth and (2) the face develops around the basicranium with significant interactions occurring during
growth at specific structural connections between these
regions [i.e., the growth counterparts defined by Enlow
(Enlow and Hunter, 1968; Enlow et al., 1969, 1971;
Enlow and McNamara, 1973; Enlow and Azuma, 1975;
Enlow, 1990].
Previous interspecific studies of anthropoids suggest
that as a result of the integration between the cranial
base and face, an increase in basicranial flexion results
in downward rotation of the orbits and posterior face
(Ross and Ravosa, 1993; Ross and Henneberg, 1995;
McCarthy, 2001; McCarthy and Lieberman, 2001) (Fig. 1).
The subsequent result is an increase in facial kyphosis
(i.e., the angular relationship of the face and cranial
vault) with increasing cranial base flexion (DuBrul and
Laskin, 1961; Biegert, 1963; Enlow and Azuma, 1975;
Ross and Ravosa, 1993; Lieberman et al., 2000; McCarthy
and Lieberman, 2001) (Fig. 1). Increasing facial kyphosis
is therefore hypothesized to increase JJH given that
downward rotation of the toothrow contrasted with a relatively stationary glenoid fossa may increase the vertical
distance from the occlusal plane to the glenoid fossa
(Ravosa et al., 2000).
Based on the observed correlations between facial orientation and cranial base flexion in anthropoids and
JJH differences between strepsirrhines and anthropoids,
Ravosa et al. (2000, p 509) hypothesized that variation
in jaw-joint height is linked to suborder differences in
relative facial height due in turn to increased encephalization, basicranial flexion, and facial kyphosis in anthropoids (Fig. 1). We conduct an interspecific analysis of
JJH, CBA, and AFK to assess whether variation in relative JJH across primates is potentially associated with
variation in these craniofacial components.
We develop two predictions building on the Ravosa
et al.’s (2000) hypothesis. Prediction One suggests that
relative JJH will increase with greater flexion in CBA.
Prediction Two suggests that relative JJH will increase
with increasing flexion in AFK. Furthermore, we examine allometric variation in these dimensions and compare these scaling patterns between primate suborders
and anthropoid infraorders. Allometric differences in
JJH among these clades may provide important insight
into evolutionary changes in masticatory function that
occurred with the rise of these higher-order primate
clades (Ravosa et al., 2000).
1
It is important to note that significant interspecific correlations
between relative brain size and flexion are not necessarily replicated
within primate species during ontogeny (Bjork, 1955; Jeffery and
Spoor, 2002, 2004; Jeffery, 2003). During certain periods of ontogeny,
an association is not evident or can even be reversed (i.e., cranial
base extension with increasing brain size) indicating the multifactorial nature of primate cranial base growth (Sirianni and Swindler,
1979; Lieberman et al., 2000; Jeffery, 2003).
2
We want to clarify that we are not excluding facial growth from
influencing basicranial form during early ontogeny (Lieberman et
al., 2000, 2008; Jeffrey and Spoor, 2002; Bastir and Rosas, 2006;
Bastir et al., 2006), but rather focusing on one aspect of a multifactorial relationship. Our correlational analysis cannot discriminate
cause and effect in any observed association between various cranial
components.
American Journal of Physical Anthropology
MATERIALS AND METHODS
Samples and measurements
We collected data from 82 adult primate species
including 39 strepsirrhines, 17 platyrrhines, and 26
catarrhines (Appendix A). Typically, species means were
based on three to five adult males and females, respectively. Because we compiled data from literature sources,
the number of individuals per species varies across
dimensions and species means reflect measurements
taken on different individuals.
We define JJH as the vertical distance from the maxillary occlusal plane to the glenoid articular surface perpendicular to this occlusal plane (Biegert, 1963)
521
JJH ACROSS PRIMATES
Fig. 2. Measures of (a) jaw-joint height (Vinyard, 1999), (b)
cranial base angle (Lieberman and McCarthy, 1999), and facial
kyphosis (Ross and Ravosa, 1993).
(Fig. 2a). The maxillary occlusal plane is defined by a
straight line passing through the tips of the anterior
maxillary premolar and the posterior cusp of the last
maxillary molar. Similar to the posterior facial height
measurement of Bastir and Rosas (2004), JJH attempts
to capture the vertical height of the posterior face. We
measured JJH from lateral-view video captures using
SigmaScan Pro 4.0 software (SPAA, Inc.).
CBA and AFK angles were taken from data provided
in Lieberman et al. (2000) based on lateral-view radiographs (Fig. 2b). We adopted the angle from basion-sellaforamen caecum as an estimate of basicranial angulation
(Lieberman and McCarthy, 1999). We used this estimate
of basicranial angulation, because the distance from sella
to foramen caecum only captures variation in the anterior cranial floor, and this distance contributes to growth
counterparts related to both the upper and mid-face
(Enlow, 1990; Spoor, 1997; Lieberman and McCarthy,
1999). Facial kyphosis is estimated as the angle formed
by the intersection of the planes of the clivus and the
floor of the nasal fossa (Hofer, 1952; Ross and Ravosa,
1993; Lieberman et al., 2000).
Ten additional skull measurements were collected and
used to generate a geometric mean (GM) for estimating
overall skull size. Species means are provided in
Appendix A.
Analyses
Linear measurements were natural log transformed
before analysis to improve linearity and reduce sizerelated heteroscedascity. Given our broad interspecific
sampling, size differences across primate species repre-
sent a key intervening factor potentially influencing
relationships among these craniofacial dimensions.
Because our goal is to examine structural relationships
between skull elements, we used a GM of several skull
measurements (Appendix A) to estimate overall skull
size (Vinyard, 2008).
We examined scaling patterns for JJH, CBA, and AFK
relative to this cranial size estimate using least squares
(LS) and reduced major axes (RMA) regressions. We calculated the RMA 95% confidence interval using the LS
confidence interval (Sokal and Rohlf, 1995). Scaling patterns were examined in both suborders and separately
for platyrrhines and catarrhines. We used analyses of covariance (ANCOVA) relative to the skull GM to compare
scaling patterns for JJH and CBA between suborders
and the two anthropoid infraorders. We used ANOVA to
compare AFK among these groups as AFK was not correlated with the skull GM.
To test Predictions One and Two from Ravosa et al.
(2000), we calculated semipartial product-moment correlations between relative JJH and both CBA and AFK. In
these semipartial correlations, relative JJH is estimated
as the residuals from a LS regression of JJH on the skull
GM across our entire primate sample.3
Because primates differ in their phylogenetic relatedness, we performed analyses using independent contrasts (ICs) in addition to conventional statistical tests.
Phylogenies were taken from Smith and Cheverud
(2002) and Purvis (1995) for anthropoids and Vinyard
and Hanna (2005) for strepsirrhines (Appendix B). ICs
were performed using Compare 4.6 (Martins, 2004).
Branch lengths were set to unity to eliminate bias due
to arbitrary assignments of branch lengths for primate
taxa (Garland et al., 1992; Diaz-Uriarte and Garland,
1998). From contrast data, we estimated regressions and
correlations as outlined earlier. We performed phylogenetic ANCOVAs and ANOVAs by suborder and anthropoid infraorder following Garland et al. (1993) using the
PDSimul, PDSingle, and PDANOVA modules in PDAP.
We applied a sequential Bonferroni adjustment (a 5
0.05) due to the multiple comparisons in the regression,
ANCOVA, and ANOVA analyses (Rice, 1989).
RESULTS
Scaling patterns among primate clades
JJH among strepsirrhines shows a nonsignificant or
moderate correlation with skull size for the IC and conventional data, respectively (Table 1). These low correlations underlie a mixed scaling pattern where conventional and IC LS regressions suggest negative allometry,
although not excluding isometry, while the conventional
and IC RMA regressions suggest positive allometry
(Table 1, Fig. 3a). Among anthropoids, JJH scales with
strong positive allometry relative to skull size (Table 1,
Fig. 3a) [see also Ravosa et al. (2000)]. Similarly, JJH
3
Previous critiques of using residuals and ratios in size adjustment (e.g., Corruccini, 1987; Jungers et al., 1995; Smith, 2005) illustrate the importance of proper interpretation of results from these
different size-adjustment approaches. In this case, we came to similar conclusions when repeating the analysis using dimensionless
shape ratios relative to the skull geometric mean. Additionally, we
came to qualitatively similar conclusions when examining semipartial correlations calculated from clade-specific samples rather than
the primate-wide sample.
American Journal of Physical Anthropology
Nc
37
42
16
26
11
28
10
18
11
29
10
19
Cladeb
Strep
Anth
Plat
Cat
Strep
Anth
Plat
Cat
Strep
Anth
Plat
Cat
(60.61)
(60.35)
(60.63)
(60.43)
–
–
–
210.38 (611.13)
–
–
24.56 (621.48)
–
0.70
1.73
2.28
1.36
IC LS sloped,e
(60.61)
(60.35)
(60.63)
(60.43)
–
–
–
215.95 (611.13)
–
–
36.01 (621.48)
–
1.91
2.05
2.53
1.69
IC RMA sloped,e
0.37
0.85
0.90
0.80
20.01
20.25
0.45
20.65
0.37
20.07
0.68
20.23
(0.026)
(\0.001)
(\0.001)
(\0.001)
(0.99)
(0.21)
(0.19)
(0.003)
(0.27)
(0.73)
(0.03)
(0.34)
IC rf
(60.40)
(60.21)
(60.45)
(60.28)
–
27.10 (65.63)
2 9.42 (68.15)
28.40 (66.40)
–
–
21.71 (618.36)
–
0.88
1.79
2.23
1.71
LS slopee,g
81.35
190.72
139.15
193.63
21.41
24.07
25.47
23.84
(61.26)
(60.78)
(61.54)
(61.09)
–
(621.12)
(627.58)
(625.23)
–
–
(662.08)
–
LS constantg
1.46 (60.40)
1.90 (60.21)
2.37 (60.45)
1.84 (60.28)
–
215.68 (65.63)
2 13.75 (68.15)
214.70 (66.40)
–
–
31.29 (618.36)
–
RMA slopee,g
291.58
222.65
218.40
124.59
23.10
24.51
25.93
24.33
(61.26)
(60.78)
(61.54)
(61.09)
–
(621.12)
(627.58)
(625.23)
–
–
(662.08)
–
RMA constantg
0.60
0.94
0.94
0.93
20.15
20.45
0.69
20.57
0.44
20.05
0.69
20.26
(\0.001)
(\0.001)
(\0.001)
(\0.001)
(0.66)
(0.015)
(0.029)
(0.013)
(0.18)
(0.79)
(0.026)
(0.29)
rh
b
JJH, jaw-joint height (mm); CBA, cranial base angle (degrees); AFK, facial kyphosis angle (degrees).
Strep, strepsirrhines; Anth, anthropoids; Plat, platyrrhines; Cat, catarrhines.
c
N, sample size for each clade.
d
IC LS slope refers to the least-squares slope estimate (passing through the origin) based on independent contrasts (IC). IC RMA slope refers to the reduced major axis slope estimate based on contrast data. The 95% confidence intervals (CI) for the slope are provided in parentheses.
e
For JJH, italicized values denote positive allometry. Values in normal font indicate that the slope does not differ significantly from isometry.
f
IC r refers to the product-moment correlation based on independent contrasts. P values are provided in parentheses. Bold values are significant after Bonferroni adjustment at
a \ 0.05.
g
LS slope refers to the least-squares regression slope. LS constant refers to the least-squares constant. RMA slope refers to the reduced major axis slope. RMA constant refers to
the reduced major-axis constant. The 95% confidence intervals (CI) for the slope and constant are provided in parentheses.
h
r refers to the product-moment correlation. P-values are provided in parentheses. Bold values are significant after Bonferroni adjustment at a \ 0.05.
a
AFK
CBA
JJH
Dimensiona
TABLE 1. Scaling patterns for ln jaw-joint height (JJH), cranial base angle (CBA), and the angle of facial kyphosis (AFK) versus the ln skull GM for different primate clades
522
B.A. ARMFIELD AND C.J. VINYARD
American Journal of Physical Anthropology
Fig. 3. Plot of (a) ln jaw-joint height, (b) cranial base angle,
and (c) facial kyphosis on ln skull geometric mean (symbols: l,
Strepsirrhines; n, Platyrrhines; ~, Catarrhines).
scales with positive allometry in both anthropoid infraorders, although the 95% CI for the IC LS slope in catarrhines includes a possible isometric scaling pattern.
Among strepsirrhines, angular changes in the basicranium (CBA) and AFK are not correlated with skull size
523
JJH ACROSS PRIMATES
a
TABLE 2. ANCOVA and ANOVA comparisons between primate clades
IC ANCOVAc
Dimension
b
N
Slope
Anthropoids versus Strepsirrhines
JJH
42/37
Anth [ Strep
(P 5 0.02)
CBA
11/28
NS
10/18
NS
AFK
10/19
–
Constant
Slope
Constant
IC ANOVAe
ANOVAf
–
Anth [ Strep
(P \ 0.001)
NS
–
–
–
NS
–
–
–
–
NS
NS
Cat [ Plat
(P 5 0.035)
Plat [ Cat
(P 5 0.001)
–
–
–
–
–
–
–
–
NS
NS
Strep [ Anth
(P 5 0.02)
–
AFK
11/29
–
Platyrrhines versus Catarrhines
JJH
16/26
NS
CBA
ANCOVAd
NS
Plat [ Cat
(P 5 0.008)
–
See Table 1 for abbreviations. Bold values are significant (a \ 0.05) after Bonferroni adjustment.
Anthropoid sample sizes are listed first followed by strepsirrhine sample sizes. Similarly, platyrrhines are listed first followed by
catarrhines.
c
IC ANCOVA of clade differences in regression slopes and constants for ln JJH and cranial angles relative to the ln skull GM are
based on a simulated F-statistic incorporating phylogenetic nonindependence (Garland et al., 1993); NS indicates no significant
difference in slope or constant between infraorders (a 5 0.05).
d
ANCOVA of LS regressions for ln JJH and cranial angles relative to the ln skull GM between primate clades.
e
IC ANOVA of clade differences in AFK are based on a simulated F-statistic incorporating phylogenetic non-independence (Garland
et al., 1993).
f
ANOVA between primate clades for AFK.
a
b
TABLE 3. Correlations and semipartial correlations among relative ln jaw-joint height (JJH), cranial base angle (CBA), and the
angle of facial kyphosis (AFK)a
Strepsirrhines
Relative ln JJHb—CBA
Relative ln JJH—AFK
CBA—AFK
Anthropoids
Catarrhines
Platyrrhines
r
IC r
rc
IC r
r
IC r
r
IC r
20.08
(P 5 0.82)
20.28
(P 5 0.40)
0.131
(P 5 0.72)
0.23
(P 5 0.52)
0.35
(P 5 0.32)
20.12
(P 5 0.77)
0.41
(P 5 0.03)
0.38
(P 5 0.04)
0.44
(P 5 0.02)
0.52
(P 5 0.005)
0.32
(P 5 0.10)
0.34
(P 5 0.08)
0.20
(P 5 0.43)
20.01
(P 5 0.96)
0.19
(P 5 0.45)
0.09
(P 5 0.73)
20.09
(P 5 0.73)
0.24
(P 5 0.35)
0.85
(P 5 0.002)
0.85
(P 5 0.002)
0.78
(P 5 0.005)
0.73
(P 5 0.03)
0.60
(P 5 0.09)
0.53
(P 5 0.12)
a
See Table 1 for abbreviations.
Relative ln JJH takes the skull GM into account in the semipartial correlation. Relative ln JJH values are equivalent to the residuals from a least-squares regression of ln JJH on the ln skull GM across the entire primate sample.
c
Bold values are significant (a \ 0.05).
b
(Table 1, Fig. 3). Although the lack of a strong association may be related to the small strepsirrhine sample
sizes, these results follow previous observations that
these angular dimensions do not strongly covary with
skull size across strepsirrhines (Ross and Ravosa, 1993).
Conventional data suggest that the anthropoid basicranial angle tends to flex as skull size increases (Ross
and Ravosa, 1993). When accounting for phylogenetic
nonindependence, however, this correlation is no longer
apparent (Table 1). When the two infraorders are considered independently, platyrrhines show a tendency
toward size-related flattening of the basicranium while
catarrhines become more flexed with size. When phylogeny is taken into account, the correlation between CBA
and size is not significant in platyrrhines.
The degree of facial kyphosis shows little relationship
with skull size across anthropoids or catarrhines (Table 1,
Fig. 3c). Alternatively, platyrrhines show a trend (i.e., P \
0.05) toward increasing facial kyphosis with skull size.
Comparison among suborders and
anthropoid infraorders
Both conventional and IC ANCOVAs suggest that
anthropoid JJH increases significantly faster with skull
size than strepsirrhines, although the IC result does not
reach significance after Bonferroni adjustment (Table 2,
Fig. 3a) (Ravosa et al., 2000). It is apparent from Figure
3a that anthropoids (with the exception of callitrichids
and squirrel monkeys) typically have on average taller
jaw-joints than most strepsirrhines at a given skull size
(Ravosa et al., 2000). Platyrrhines and catarrhines do
not differ significantly in JJH for the IC ANCOVA, but
the conventional ANCOVA suggests that platyrrhine
JJH increases more quickly with skull size (Table 2).
Suborder comparisons for CBA demonstrate a significant difference in y-intercept for the IC data with strepsirrhines having a less-flexed cranial base (i.e., a larger
CBA angle) than anthropoids for a given skull size
American Journal of Physical Anthropology
524
B.A. ARMFIELD AND C.J. VINYARD
Fig. 5. Plot of cranial base angle on facial kyphosis (symbols: l, Strepsirrhines; n, Platyrrhines; ~, Catarrhines).
Fig. 4. Plot of relative ln jaw-joint height on (a) cranial base
angle and (b) facial kyphosis (symbols: l, Strepsirrhines; n,
Platyrrhines; ~, Catarrhines).
(Table 2, Fig. 3b). Between anthropoid infraorders, the
conventional data indicate that platyrrhine CBA
increases at a significantly faster rate than catarrhines.
When examining IC data, this slope difference is not significant; however, platyrrhines tend to have a significantly less flexed cranial base than catarrhines at a
given skull size (Table 2, Fig. 3b).
Anthropoids and strepsirrhines show no significant
differences in the AFK relative to skull size (Table 2,
Fig. 3c). Similarly, platyrrhines and catarrhines show no
statistical differences in AFK between infraorders in the
conventional or IC ANOVA (Table 2).
Correlations among relative JJH and cranial
angles
Prediction One suggests that increased basicranial
flexion will be correlated with relatively taller jaw joints
in various primate clades. Strepsirrhines show no relationship between relative JJH and CBA (Table 3, Fig.
4a). Alternatively, anthropoids show a moderate semipartial correlation for the conventional and IC data
(Table 3). These correlations, however, are positive indicating that relatively taller JJHs are associated with
less flexed cranial bases among anthropoids (Fig. 4a).
This relationship runs contrary to Prediction One.
American Journal of Physical Anthropology
Further examination indicates that the observed association between CBA and relative JJH in anthropoids
appears to be primarily related to the association of
these two variables in platyrrhines (Fig. 4a). New World
monkeys exhibit significant positive correlations between
CBA and relative JJH for both conventional and IC data
(Table 3). Alternatively, catarrhines show no statistical
relationship between these two variables.
A broadly similar pattern is seen for correlations
between AFK and relative JJH (Table 3, Fig. 4b). Prediction Two suggests that relative JJH increases with
increasing flexion in AFK. Strepsirrhines exhibit no
association while anthropoids show some evidence for a
positive association between AFK and relative JJH for
the conventional data (P \ 0.05). Like Prediction One,
this association is opposite to the predicted relationship
between these variables. The association observed across
anthropoids appears to be primarily due to the strong
positive association of AFK and relative JJH among platyrrhines (Table 3). Catarrhines show no association
between these variables.
Finally, comparisons of AFK and CBA show no
evidence of an association in strepsirrhines or catarrhines (Table 3, Fig. 5). Alternatively, anthropoids and
platyrrhines exhibit a significant correlation between
these two angles for the conventional data. Ross and
Ravosa (1993) observed similar clade-specific relationships (or lack thereof) between AFK and CBA.
DISCUSSION
We did not observe the hypothesized associations
between relative JJH and either the basicranial angle
(CBA) or AFK in the primate clades examined here. Furthermore, the three primate clades exhibited highly divergent relationships between relative JJH and these
two angles. These observations raise questions about
how clade-specific craniofacial growth influences their
respective relationships between the posterior face and
basicranium, how these patterns affect masticatory function across primates and how these clade-specific morphological patterns arose during primate evolution.
525
JJH ACROSS PRIMATES
(Ross and Ravosa, 1993; Lieberman et al., 2000; Ross,
2000; McCarthy, 2001; Ross et al., 2004). First, JJH in
primates appears to be influenced by multiple factors
including those that impact CBA and facial angle
(Ravosa et al., 2000; Bastir and Rosas, 2004; Lieberman
et al., 2000, 2008). This mosaicism is clearly apparent in
the interspecific data examined here, and we speculate
that the interspecific pattern translates from the multifactorial set of influences that occur during growth
within primates (Enlow, 1990; Jeffery, 2003, Bastir
and Rosas, 2004; Lieberman et al., 2008). Second, these
influences likely changed throughout the evolution of different primate lineages. This evolutionary divergence is
most evident in the differences in JJH and CBA between
primate suborders (Table 2; Figs. 3 and 6a). Finally, the
mosaicism indicates that we are unlikely to identify a
single satisfying structural explanation for the observed
interspecific variation in JJH, or by extension posterior
facial height, among primates. Future analyses may benefit from considering phylogentically restricted groups of
primates to highlight how changes in growth and integration patterns influence JJH in these restricted primate clades (e.g., Bastir and Rosas, 2004, 2005).
Strepsirrhines
Fig. 6. (a) Scatterplot of ln jaw-joint height on cranial base
angle in primates. (b) Boxplot of ln jaw-joint height for strepsirrhines, platyrrhines, catarrhines, and specific fossil primates.
Jaw-joint heights for fossil specimens were measured as
described in the methods using scaled lateral-view photographs
of the specimens published in the primary literature (symbols:
l, Strepsirrhines; n, Platyrrhines; ~, Catarrhines).
The mosaic pattern of JJH relationships in
different primate clades
We observed disparate patterns of correlations and
scaling relationships for JJH relative to midline basicranial and facial angles among primate clades. Strepsirrhines differ from anthropoids in having on average lessflexed basicrania and absolutely shorter JJH (Fig. 6a).
Within both strepsirrhines and catarrhines, however, relative JJH is unrelated to CBA and AFK. Platyrrhines
show a third pattern where relatively taller JJH is correlated with less-flexed basicrania and to a lesser extent
more airorhynch faces. These differing relationships
extend earlier observations that cranial base morphology
exhibits a number of different relationships with facial
form across primate clades and has several implications
JJH in strepsirrhines shows at best a modest correlation with skull size and essentially no relationship with
the midline CBA and facial angle (Tables 1 and 3). There
are potentially several, nonmutually exclusive, explanations for this lack of association. In part, the small strepsirrhine samples for CBA and AFK likely contribute.
More interestingly, the weak correlations across strepsirrhines may be partly due to differing relationships
among strepsirrhine families. For example, cheirogaleids
trend toward an absolute decrease in JJH with increasing skull size in contrast to most other strepsirrhine
families. This tendency is largely due to the absolutely
low-condyle position and large size of Phaner furcifer
among cheirogaleids. In this instance, the pattern may
be attributable to lowering of JJH in conjunction with
increased gapes during tree gouging in this largest member of the clade (Vinyard et al., 2003). Galagonids show
a less-striking, but similar pattern. The largest genus,
Otolemur, also exhibits relatively low-condyle heights
and feeds extensively on exudates (Williams et al., 2002;
Burrows and Smith, 2005).
Regardless of explanation, the observed lack of association among strepsirrhines recapitulates observations
seen in previous studies examining CBA and facial morphologies (Ross and Ravosa, 1993). It is interesting to
speculate that the lack of interspecific association may
result from a lack of integration among these basicranial
and facial components within strepsirrhine species.
Because JJH has specific functional implications related
to mastication, low levels of integration in strepsirrhines
may indicate a relative ‘‘freedom’’ for independent evolution of JJH and posterior facial height when compared
with many anthropoid species. Concomitantly, variation
in strepsirrhine JJH may be more closely related to
functional demands over integrated changes in cranial
base-face architecture (Ravosa et al., 2000).
Anthropoids: platyrrhines vs. catarrhines
Anthropoid JJH scales with positive allometry relative
to skull size (Table 1; Fig. 3a). Beyond this suborder
American Journal of Physical Anthropology
526
B.A. ARMFIELD AND C.J. VINYARD
scaling pattern, platyrrhines and catarrhines diverge
markedly in their relationships between JJH and the
two craniofacial angles. Platyrrhines exhibit moderate
associations between relative JJH and both CBA and
AFK, whereas catarrhines show no relationships (Table
3; Fig. 4). Thus, the significant correlations among relative JJH, CBA, and AFK in anthropoids appear to result
primarily from the relationships in New World monkeys
(Table 3). The significant associations in platyrrhines
still fail to support our predictions as both the cranial
base and face become less, rather than more, flexed with
relatively larger JJH.
As typical of interspecific comparisons, the associations
between relative JJH and both the basicranial and facial
angles in platyrrhines may result from multiple underlying effects. These factors may impact all species in a
clade or significant interspecific associations can arise
from specific evolutionary events affecting one or two
clades within the larger group. Among platyrrhines, the
derived craniofacial configuration of howlers, potentially
related to their enlarged hyoid apparatus and folivory
(Beigert, 1963; Zingeser, 1973), and callitrichids, related
to the reduced condylar height in the tree-gouging
pygmy marmoset, extend the platyrrhine distribution
(Figs. 4 and 5). Removing these extremes, however, does
not alter the basic pattern observed across platyrrhines,
suggesting that the group may share significant associations among these craniofacial variables not found in
other primate clades.4
The differences between platyrrhine and catarrhine
skulls likely extend beyond the dimensions examined
here as both CBA and AFK exhibit dissimilar relationships with skull size between the two clades (Ross and
Ravosa, 1993) (Table 1; Fig. 3). For example, Bouvier
(1986) identified several morphological differences in the
masticatory apparatus of platyrrhines relative to catarrhines. Combining these results suggest that infraorder
differences in craniofacial angles or masticatory apparatus form may be indicative of a larger pattern of
disparity in craniofacial morphology between the two
anthropoid infraorders. If true, then these differences in
morphology imply that the two clades have experienced
distinct evolutionary pressures on craniofacial form since
their split from a common ancestor. Future work is
needed to compare skull form in greater detail between
these two infraorders.
Finally, the different relationships among JJH, CBA,
and AFK between platyrrhines and catarrhines raise an
important consideration for interspecific studies across
anthropoids. A key concern questions whether catarrhine and platyrrhine skulls differ sufficiently that combining them in a single group for analysis can mislead
interpretations of skull form in the two infraorders.
Although studies have demonstrated infraorder differences (e.g., Bouvier, 1986; Ross and Ravosa, 1993), conclusions based on combined analyses of catarrhine and platyrrhine species have also been common (e.g., Ravosa
et al., 2000). On the basis of our results, we argue that
additional analyses comparing platyrrhines and catarrhines might further our understanding of the evolutionary history of the anthropoid radiation.
4
We acknowledge that we cannot rule out the converse pattern
that some catarrhines, such as the Old World monkeys (e.g., Delson
and Rosenberger, 1984), possess a canalized craniofacial form underlying their lack of association among these variables.
American Journal of Physical Anthropology
The primate posterior face and its relationships
with the midline versus lateral cranial base
Recently, Bastir and colleagues have shown that the
posterior face in humans and chimpanzees shares a
stronger morphological association with the lateral compared to the midline basicranium (Bastir and Rosas,
2004, 2005, 2006; Bastir et al., 2004, 2006). Midline basicranial features are associated with the posterior face,
however, these correlations tend to be weaker than those
involving the lateral basicranium. As noted by Enlow
(1990, p 209), the stronger association between the lateral basicranium and posterior face is not unexpected
given that the actual contacts between growth counterparts involve lateral structures in the skull. Additionally,
Bastir and Rosas (2006) hypothesize that the stronger
association between the posterior face and lateral basicranium partly reflects their overlapping growth periods,
providing greater opportunity for growth-related interactions, while the midline cranial base completes most of
its growth earlier in ontogeny (Bastir and Rosas, 2006).
Thus, our use of midline basicranial structures provides
a convenient set of landmarks for comparative analysis,
but may have a less direct relationship with the posterior face during growth.
The observation that the posterior face may share
more growth-related interactions with the lateral basicranium in hominoids has several implications for our
results. First, while we demonstrate correlations
between midline craniofacial angles and relative JJH,
there may be stronger associations between relative JJH
and the lateral basicranium. This hypothesis deserves
further investigation to determine whether patterns
observed in chimpanzee and human basicrania are found
throughout primates. Second, differing patterns of integration between the midline and lateral basicranium
may help explain the discordant results found between
higher-order primate clades in this study as well as previous analyses of basicranial and facial form (Ross and
Ravosa, 1993; Jeffery, 2003). As a hypothetical example,
platyrrhines may exhibit higher levels of integration
between midline and lateral basicranial structures,
which may subsequently underlie the significant associations between midline basicranial angulation and relative JJH in this clade. Third, the varying pattern of
results across these major primate clades suggests that
primates do not show a single pattern of integration
between the basicranium and face. Extrapolating results
from analyses of single species or single clades to primates as an order is a risky endeavor at best. Additional
data from the basicranium, in particular, lateral structures, across a broader sample of primates are needed to
address these issues.
Functional implications for patterns of JJH
variation
Anthropoids on average have taller JJHs for a given
skull size than strepsirrhines (Ravosa et al., 2000),
whereas catarrhines exhibit a slight tendency to have
relatively taller JJHs than platyrrhines (Table 2).
Because JJH increases with positive allometry, these
transpositions may be a consequence of the average
larger size of anthropoids over strepsirrhines and catarrhines over platyrrhines (Fig. 3a). A relatively taller
JJH has been argued to enhance masseter and medial
pterygoid size and potentially moment arm lengths
527
JJH ACROSS PRIMATES
(Greaves, 1974; Ward and Molnar, 1980; Freeman, 1988),
more evenly distribute occlusal forces along the postcanine tooth row (Zingeser, 1973; Greaves, 1974; Ward and
Molnar, 1980) and result in a more vertically-oriented
masseter and medial pterygoid muscle resultant (Ravosa
et al., 2000). Thus, size-correlated changes in relative
JJH likely have specific functional consequences for masticatory behaviors across primates (Zingeser, 1973;
Greaves, 1974, 1980, 1995; Herring and Herring, 1974;
Osborn, 1987; McCollum, 1999; Ravosa et al., 2000; Sondang et al., 2003; Vinyard et al., 2003).
The mosaic pattern of correlations and scaling relationships for JJH across different primate clades may
indicate that the primate infraorders have experienced
distinct functional demands related to feeding performance. Alternatively, variation in JJH may reflect correlated shifts in facial height resulting from evolutionary
changes in CBA and facial angle throughout primate
evolution (Ravosa et al., 2000). With the exception of
platyrrhines, it does not appear that relative JJH is
fundamentally linked to variation in basicranial and
facial angulation across primates contrary to Ravosa et
al. (2000). In the previous section, we argued that the
potentially low levels of integration between JJH and
craniofacial angulation in strepsirrhines may provide
them a relative ‘‘freedom’’ for independent evolution of
JJH compared to anthropoids. We can extend this
argument to include catarrhines when compared with
platyrrhines. In doing so, we generate a hypothesis
predicting stepwise differences in the levels of integration between posterior facial height and craniofacial
angulation across primates. Testing this hypothesis
will help us to better understand the relative roles of
size-related, developmental and dietary influences on
posterior facial height in these different primate
clades.
Evolution of JJH in primates
Anthropoids have diverged from strepsirrhines in several craniofacial features, including aspects of their masticatory apparatus and neurocranial dimensions linked
to housing larger brains (Ross, 1996; Kay et al., 1997).
The masticatory apparatus of anthropoids tends to exhibit more robust corpora (including fused symphyses),
greater isognathy (i.e., the widths of upper and lower
dental arcades are more similar), relatively large molar
crushing surfaces, relatively isodontic molars (i.e., the
upper and lower molars have more similar widths), and
more vertically-oriented superficial masseters compared
to the average strepsirrhine (Hiiemae and Kay, 1973;
Kay, 1975; Hylander, 1979; Ravosa, 1991, 1999; Ravosa
and Hylander, 1994; Ravosa et al., 2000; Ross, 2000).
The vertically-oriented superficial masseters are linked
to relatively tall mandibular rami and JJHs that also
characterize anthropoids (Ravosa et al., 2000). Although
the relatively taller JJH have specific functional consequences for mastication, it remains unclear whether
changes in anthropoid facial heights reflect masticatory
adaptations and/or correlated effects resulting from morphological shifts in other cranial regions.
Anthropoids have on average both taller JJHs and
more flexed basicrania (CBA) than most strepsirrhines
at a given skull size (Figs. 3 and 6a) (Ross and Ravosa,
1993; Ravosa et al., 2000). Suborder differences in both
JJH and CBA support the hypothesis that changes in
basicranial angulation in stem anthropoids may have
significantly influenced facial height and masticatory apparatus function in this clade (Ravosa et al., 2000). Additionally, JJH estimates in Parapithecus grangeri, an
early anthropoid (Fleagle and Kay, 1987), and Rooneyia
viejaensis, and an enigmatic Eocene fossil demonstrating
anthropoidlike features (Szalay and Wilson, 1976; Rosenberger, 2006), are intermediate between strepsirrhines
and anthropoids further supporting the plausibility of
this evolutionary scenario (Fig. 6b). We lack the necessary data on CBA in early anthropoids to assess whether
CBA and JJH are evolving simultaneously as further
assessment of the hypothesis that cranial base flexion
initiated a cascade of developmental events resulting in
the taller posterior facial heights observed in anthropoid
primates (Ravosa et al., 2000).5
Our hypothesis tests demonstrate little support for the
predicted relationship between increased relative JJH
and cranial base flexion in primates. In fact, platyrrhine
primates show the strongest relationship between these
dimensions, but increases in relative JJH are correlated
with less-flexed CBA throughout the clade. Our results
suggest that if the observed differences in JJH between
anthropoids and strepsirrhines are related to CBA, then
this evolutionary event may have been limited to a relatively brief period at the origin of anthropoids. From a
comparative perspective, we could hypothesize this distinct event as creating a ‘‘grade shift’’ in JJH between
strepsirrhines and anthropoids. Failure to observe the
predicted relationship between relative JJH and CBA
across anthropoids suggests that these two features have
been influenced by additional, and in many cases independent, factors during the evolution of the anthropoid
infraorders. The stem catarrhine Aegyptopithecus zeuxis
possesses an intermediate JJH that falls at the lower
end of the catarrhine range of values (Fig. 6b) and may
help establish the longevity of these distinct influences
on the anthropoid infraorders. Although this speculation
is interesting, additional work in fossil primates is
needed to document the history of morphological changes
in JJH and cranial angulation throughout anthropoid
evolution.
ACKNOWLEDGMENTS
We thank the following institutions and individuals for
providing access to primate skulls: Field Museum of Natural History (L. Heaney, B. Patterson, and W. Stanley);
National Museum of Natural History (L. Gordon and R.
Thorington); American Museum of Natural History (R.
MacPhee); Natural History Museum, London (P. Jenkins); Muséum National d’Histoire Naturelle (J. Cuisin);
Naturhistorisches Museum Basel (M. Sutermeister and
F. Weidenmayer). B. Shea and D. Schmitt kindly allowed
access to video capture and videometric analysis software. We thank two anonymous reviewers for numerous
helpful comments that improved the manuscript.
5
Simons (2004) reports an estimated cranial base angle of 1578 for
a single P. grangeri specimen (DPC 18651). Measurement details
are not provided. Thus, we cannot directly compare this value to
those used here. Simons (2004) does however indicate that this
value for P. grangeri falls at the flexed end of the strepsirrhine
range (1578–1818) and within the anthropoid range (1358–1888)
based on comparison with data from Ross and Ravosa (1993).
American Journal of Physical Anthropology
528
B.A. ARMFIELD AND C.J. VINYARD
APPENDIX A
TABLE A1. Primate species and measurements included in the analysis
Species
Cheirogaleus major
Cheirogaleus medius
Microcebus murinus
Microcebus rufus
Mirza conquereli
Phaner furcifer
Avahi laniger
Indri indri
Propithecus diadema
Propithecus verreauxi
Eulemur coronatus
Eulemur fulvus
Eulemur macaco
Eulemur mongoz
Eulemur rubriventer
Hapalemur griseus
Hapalemur simus
Lemur catta
Varecia variegata
Lepilemur dorsalis
Lepilemur edwardsi
Lepilemur leucopus
Lepilemur microdon
Lepilemur mustelinus
Lepilemur ruficaudatus
Lepilemur septentrionalis
Arctocebus aureus
Arctocebus calabarensis
Galago alleni
Galago gallarum
Galago matschiei
Galago moholi
Galago senegalensis
Galagoides demidoff
Galagoides zanzibaricus
Otolemur crassicaudatus
Otolemur garnetti
Callimico goeldii
Callithrix humeralifer
Cebuella pygmaea
Leontopithecus rosalia
Saguinus fuscicollis
Alouatta palliata
Alouatta seniculus
Aotus vociferans
Ateles chamek
Brachyteles arachnoides
Callicebus cupreus
Cacajao melanocephalus
Cebus apella
Chiropotes satanas
Lagothrix lagotricha
Pithecia pithecia
Saimiri sciureus
Allenopithecus nigroviridis
Cercopithecus aethiops
Cercocebus torquatus
Cercopithecus mitis
Erythrocebus patas
Lophocebus albigena
Macaca fascicularis
Macaca nemestrina
Mandrillus leucophaeus
Miopithecus talapoin
Papio anubis
Theropithecus gelada
Colobus guereza
Nasalis concolor
Family
JJHa
CBAb
AFKb
Cheirogaleidae
Cheirogaleidae
Cheirogaleidae
Cheirogaleidae
Cheirogaleidae
Cheirogaleidae
Indriidae
Indriidae
Indriidae
Indriidae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Lemuridae
Megaladapidae
Megaladapidae
Megaladapidae
Megaladapidae
Megaladapidae
Megaladapidae
Megaladapidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Lorisidae
Callitrichidae
Callitrichidae
Callitrichidae
Callitrichidae
Callitrichidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cebidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Cercopithecidae
Colobinae
Colobinae
2.41
1.18
2.67
2.10
2.61
0.813
5.57
10.14
9.78
8.04
3.99
4.22
5.37
4.60
5.17
3.35
8.64
5.45
4.25
4.66
5.17
4.14
4.28
4.26
4.25
4.50
4.37
3.47
4.18
2.85
2.77
3.85
3.04
2.99
3.70
3.52
2.07
6.96
3.29
1.29
6.74
2.52
28.15
32.65
6.70
11.78
21.80
7.04
9.37
9.49
9.72
13.90
7.56
2.42
13.61
10.14
20.03
11.82
8.59
17.86
15.69
18.03
27.22
7.57
22.15
39.90
16.76
10.24
186.8
154
142.8
189
138.2
183.7
186.2
153.2
166.3
184.8
137
183.7
158
179.5
144.2
187.8
181.2
143.2
194.4
156.7
178.7
155.8
165
141.5
164.2
172.5
164.5
180.7
141.5
154.5
140
174.8
172.5
159.4
166.6
169.5
176
175.8
165.5
154.2
169.9
151.4
162
135.3
157.3
170
158.7
161.5
142
142.8
134.8
163.8
155
164.2
153.2
156.5
130.6
150
175.3
146.8
160.2
160.8
SkullGMc
21.74
16.17
11.87
12.20
19.46
20.23
21.68
40.76
36.26
33.25
31.40
35.40
36.06
32.06
35.76
26.75
36.40
31.72
42.33
22.13
22.58
19.95
22.85
23.63
22.60
21.59
18.25
21.25
19.35
16.61
15.88
15.40
16.62
13.24
16.08
27.57
26.21
.
18.73
13.38
22.79
18.79
44.42
46.57
23.68
41.53
46.58
24.70
34.34
38.80
31.99
40.03
29.71
22.28
38.82
39.46
51.66
40.29
48.51
46.06
45.93
52.66
71.01
26.38
72.15
67.42
45.91
39.74
(continued)
American Journal of Physical Anthropology
529
JJH ACROSS PRIMATES
TABLE A1. (Continued)
Family
JJHa
Colobinae
Colobinae
Colobinae
Colobinae
Colobinae
Colobinae
Colobinae
Hylobatidae
Hylobatidae
Hominidae
Hominidae
Hominidae
13.94
8.67
11.97
10.08
14.55
15.78
11.32
12.41
18.44
65.50
32.73
64.22
Species
Nasalis larvatus
Presbytis rubicunda
Procolobus rufomitratus
Procolobus verus
Pygathrix nemaeus
Rhinopithecus roxellana
Trachypithecus obscura
Hylobates lar
Hylobates syndactylus
Gorilla gorilla
Pan troglodytes
Pongo pygmaeus
CBAb
AFKb
SkullGMc
159
166.5
171.4
156.1
157.2
161.3
143.8
161
154.5
143.5
143.8
168.3
158.3
157.3
158.7
160.8
150.2
123
138.8
46.96
36.51
41.78
34.67
43.13
47.20
39.85
39.98
48.67
100.13
75.30
91.54
a
Jaw-joint height (JJH) taken from Vinyard (1999). Values are in mm.
Cranial base angle (CBA) and the angle of facial kyphosis (AFK) were taken from Lieberman et al. (2000). Values are in degrees.
c
The skull geometric mean (SkullGM) is based on the following linear dimensions taken from Vinyard (1999): (1) mandible length,
(2) palate length, (3) nasion–prosthion height, (4) cranial length, (5) bizygomatic breadth, (6) biglenoid breadth, (7) M1 width, (8)
basion–nasion length, (9) palate breadth at M1, and (10) mandibular arch breadth at M1. Values are in mm.
b
APPENDIX B
Composite phylogeny used in phylogenetic comparative analyses. Phylogenies were adapted from Purvis
(1995), Smith and Cheverud (2002) and Vinyard and
Hanna (2005). Phylogeny in Nexus format.
((((((G.matschiei,(G.alleni,(G.zanzibaricus,G.demidoff))),
(G.moholi,(G.gallarum,G.senegalensis))),(O.garnetti,
O.crassicaudatus)),(A.aureus,A.calabarensis)),((((L.
septentrionalis, (L.ruficaudatus,(L.leucopus,(L.edwardsi,
L.dorsalis)))),(L.mustelinus,L.microdon)),((V.variegata,
((L.catta,(H.griseus,H.simus)),(E.rubriventer,((E.fulvus,
E.mongoz),(E.macaco,E.coronatus))))),(A.laniger,(I.indri,
(P.diadema,P.verreauxi))))),(P.furcifer,((M.conquereli,
(M.murinus,M.rufus)),(C.major,C.medius))))),(((A.vociferans,
(((C.pygmaea,C.humeralifera),(L.rosalia,S.fuscicollis)),
(C.apella,S.sciureus))),((C.albicans,(C.satanas,(C.melanocephalus,P.pithecia))),((B.arachnoides,(A.chamek,L.
lagotricha)),(A.palliata,A.seniculus)))),((((A.nigroviridis,
(C.mitis,(M.talapoin,(C.aethiops,E.patas)))),((M.fascicularis,
M.nemestrina),((M.leucophaeus,C.torquatus),(L.albigena,
(T.gelada,P.anubis))))),((C.guereza,(P.versus,P.rufomitratus,)),
(((P.rubicunda,,T.obscurus),(N.larvatus,N.concolor)),(P.nemaeus,
R.roxellana)))),((H.lar,H.syndactylus),(P.pygmaeus,(G.gorilla,
P.troglodytes))))))
LITERATURE CITED
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