Basicranial flexion, relative brain size, and facial kyphosis in

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 91:305-324 (1993)
Basicranial Flexion, Relative Brain Size, and Facial Kyphosis
in
-.
Nonhuman Primates
CALLUM F. ROSS AND MATTHEW J. RAVOSA
Department of Biological Anthropology and Anatomy, Duke Uniuersity
Medical Center, Durham, North Carolina 27710
KEY WORDS
Encephalization,
Klinorhynchy,
Anthropoid origins, Hominid evolution
Haplorhini,
ABSTRACT
Numerous hypotheses explaining interspecific differences in
the degree of basicranial flexion have been presented. Several authors have
argued that an increase in relative brain size results in a spatial packing
problem that is resolved by flexing the basicranium. Others attribute differences in the degree of basicranial flexion to different postural behaviors,
suggesting that more orthograde animals require a ventrally flexed pre-sella
basicranium in order to maintain the eyes in a correct forward-facing orientation. Less specific claims are made for a relationship between the degree of
basicranial flexion and facial orientation. In order to evaluate these hypotheses, the degree of basicranial flexion (cranial base angle), palate orientation,
and orbital axis orientation were measured from lateral radiographs of 68
primate species and combined with linear and volumetric measures as well as
data on the size of the neocortex and telencephalon. Bivariate correlation and
partial correlation analyses at several taxonomic levels revealed that, within
haplorhines, the cranial base angle decreases with increasing neurocranial
volume relative to basicranial length and is positively correlated with angles
of facial kyphosis and orbital axis orientation. Strepsirhines show no significant correlations between the cranial base angle and any of the variables
examined. It is argued that prior orbital approximation in the ancestral haplorhine integrated the medial orbital walls and pre-sella basicranium into a
single structural network such that changes in the orientation of one necessarily affect the other. Gould’s (“Ontogeny and Phylogeny.” Cambridge:
Belknap Press, 1977)hypothesis, that the highly flexed basicranium of Homo
may be due to a combination of a large brain and a relatively short basicranium, is corroborated. o 1993 Wiley-Liss, Inc.
Tarsiers and the extant hominoids, including Homo, differ from most other mammals in having a highly flexed basicranium.
A flexed basicranium is one in which the
pre- and post-sella portions of the cranial
base are downwardly or ventrally deflected
relative to each other so that the endocranial and/or exocranial surfaces of those
bones do not lie in a single plane, but form a
ventrally open angle of less than 180” with
each other (Fig. 1).
The bony basicranium and the chondrocranium in which it forms are structurally
0 1993 WILEY-LISS, INC.
associated with the neurocranium, inner
ear, and the roof and walls of the nasal fossa
and orbits, as well as articulating with the
vertebral column. Consequently, alterations
in chondrocranial and basicranical morphology must reflect changes in these functional
matrices (Moss, 19721,and it is possible that
the basicranium transmits the effects of
changes in any one area of the skull to numerous other regions.
Received June 14,1991; accepted August 11,1992
306
C.F. ROSS AND M.J. RAVOSA
Fig. 1. A comparison of schematic cranial hemisections illustrating correspondence between an increasingly flexed basicranium and increasing size of the
brain or brain parts (large clear arrows), change in foramen magnum orientation (small arrows), and orbital
axis orientation (large solid arrows). Taxa are, from top
to bottom, Tuna, Pun, Austrulopithecus, Homo (modified
from Aiello and Dean, 1990.)
This possibility has important implications, both for the use of evidence from craniofacial morphology in phylogenetic analyses, and for adaptive and functional
interpretations of craniofacial form. Phylogenetic analyses that invoke parsimony to
select a pattern of relationships assume that
the characters that are used have evolved
independently of each other. If characterstate changes in several of these characters
can be accounted for with reference to a single underlying mechanism, then scoring
them independently may unjustly bias the
analysis.
More importantly, the possibility that
the effects of selection on one part of the
skull can be transmitted to other areas
in the skull via the basicranium must
be considered when developing adaptive
explanations for interspecific differences
in craniofacial form. Basicranially mediated structural interdependence may confound functional interpretations of correlated changes in different parts of the skull
during ontogeny and phylogeny. The separation of functional from purely structural
determinants of form is a necessary prerequisite to adaptive interpretations of craniofacial morphology.
In light of these considerations, it is
hardly surprising that the basicranium has
featured prominently in discussions of primate phylogenetic relationships (Dean and
Wood, 1981, 1982, 1984; Maier and Nkini,
1984; Shea, 1985, 1988) and craniofacial
adaptations (Demes, 1985; Shea, 1985,
1988; Lugoba and Wood, 1990).Adaptive explanations for the evolution of pronounced
basicranial flexion in hominids have usually
emphasized a correlation between the tendency to extreme basicranial flexion and
other “uniquely”human traits, such as bipedal locomotion, pronounced orthognathy, a
relatively large brain, and the capacity for
encoded speech. The main aim of the research reported here is to evaluate some of
these adaptive hypotheses by determining
whether tendencies toward highly flexed basicrania in nonhuman primates are correlated with human-like tendencies in posture
andlor the relative sizes of the brain and
masticatory apparatus.
BASICRANIAL FLEXION IN PRIMATES
HYPOTHESES
307
Biegert’s hypothesis (1963, p. 122) preAdaptive explanations for differences in dicts that large animals (like Alouatta) will
basicranial flexion (bending of the cranial have flat basicrania and small animals (like
base so that it is ventrally concave) fall into Saimiri) will have flexed basicrania, merely
three groups. Neural hypotheses relate dif- as a consequence of body size a l o n e t h e
ferences in basicranial flexion to differences masticatory apparatus scaling with positive
in total brain size or in the size of specific allometry and the neocortex with negative
parts of the brain. Postural hypotheses ex- allometry against body size. However, he
plain differences in basicranial flexion by suggests that this general allometric princihypothesizing how postural differences be- ple “can be circumvented if a specialized extween species necessitate different basicra- pansion of the neopallium (compare Ateles
nial morphologies. Facial-orientation hy- and Alouatta) or a specialized reduction of
potheses suggest a relationship between the the masticatory apparatus occurs (compare
degree of basicranial flexion and the orien- Homo with Pongidae)” (Biegert, 1963, pp.
tation of the face. These hypotheses are dis- 122-123). This predicts that size-corrected
values for neocortical volume and the size of
cussed a t greater length below.
the masticatory apparatus should be correlated with size-corrected values for the CBA.
Neural hypotheses
In addition to these general trends BiegSpatial-packing hypotheses
ert argued that a large neocortex relative to
Numerous authors have suggested that the size of the masticatory apparatus should
phylogenetic increase in relative brain size, be correlated with a n increase in the degree
or encephalization, causes a “spatial pack- of basicranial flexion, while a small neocoring“ problem that is solved by flexing the tex relative to masticatory apparatus size
basicranium-the cranial base anterior to should be associated with a less flexed basisella being deflected ventrally, or down- cranium.
The second version of the spatial-packing
ward, and the foramen magnum and postsella cranial base being displaced anteriorly hypothesis is Goulds (1977) suggestion that
to accommodate the expanding brain (Fig. 1) increased brain size relative to the length of
(e.g., Virchow, 1857; Ranke, 1892; Cameron, the basicranium is the most important
1924, 1925, 1926; Dabelow, 1931; Biegert, cause of increased basicranial flexion and
1957; Delattre and Fenart, 1963; Gould, other “paedomorphic“ features characteris1977). Differences of opinion as to what tic of the human skull (see also Vogel, 1964).
brain size should be evaluated against in In support of this hypothesis Gould cited oborder to determine its degree ofencephaliza- servations that human-like features of skull
tion underlie two slightly different versions form result when the spheno-occipital synchondrosis, a n important growth site in the
of the spatial-packing hypothesis.
The first is Biegert’s spatial-packing hy- basicranium, is excised in growing rats (Dupothesis. Biegert (1963) proposed that the Brul and Laskin, 19611, or is pathologically
extent of basicranial flexion decreases with missing in a mangabey specimen (Vogel,
increasing size of the masticatory apparatus 1964)or chicken embryos (Riesenfeld, 19691.
and increases with increasing neocortical Gould’s spatial-packing hypothesis predicts
volume. Thus, he predicts a negative correla- that animals with large brains relative to
tion between the degree of basicranial flex- the length of the bony basicranium should
ion and the size of the neocortex, and a posi- have more flexed basicrania than animals
tive correlation between the degree of basic- with relatively small brains.
ranial flexion and the size of the masticatory
apparatus ( a negative correlation between Cerebellum hypothesis
the cranial-base angle [CBA] and another
variable being one in which the angle becomes
Some workers have suggested th a t a n insmaller and the basicranium more flexed as crease in the size of the cerebellum may act
to shift the foramen magnum and post-sella
the value of the other variable increases).
308
C.F. ROSS AND M.J. RAVOSA
orbits form the floor of the anterior cranial
fossa. In such a situation ventral flexion of
the orbital axis resulting from the assumption of upright posture must necessarily result in ventral flexion of the floor of the anterior cranial fossa. Dabelow then argued
that the resulting basicranial flexion caused
an increase in brain size in primates by providing new volume into which the cerebrum
could expand.
Postural hypothesis
The primates offer us several instances in
Extreme basicranial flexion in humans which to test Dabelow’s version of the poshas often been attributed to an habitual or- tural hypothesis. Primates are characterthograde posture. The center of mass of the ized by great variation in postural habits as
head lies in front of the occipital condyles in well as great variation in the extent of basiprimates, as it does in all mammals cranial flexion and orbital axis orientation
(Schultz, 1942). This situation is assumed (Cartmill, 1970, 1972; Ravosa, 1991). Moreby advocates of the postural hypothesis to be over, haplorhines are distinguished from
biomechanically inefficient in animals with most strepsirhines in having bony orbits
an orthograde posture, an assumption that which are highly convergent and closely apappears to be bolstered by observations that proximated in the midline (Cartmill, 1970,
the foramen magnum in extant and fossil 1972). Within the Old World monkey radiahominids is positioned more anteriorly tion, colobines have a relatively broader in(Bolk, 1909; Schultz, 1942, 1955; Ashton terorbital region than cercopithecines (Deland Zuckerman, 1952, 1956; Ashton, 1957; son, 1975). If Dabelow’s postural hypothesis
DuBrul, 1977, 1979; Dean and Wood, 1981, is correct then haplorhines and cercopithe1982) and faces more ventrally (Duckworth, cines should exhibit a higher correlation be1915; Bolk, 1910; Moore et al., 1973; Adams tween the degree of basicranial flexion and
and Moore, 1975) than in other hominoids. the angle of orbit orientation relative to the
The postural hypothesis suggests that in or- post-sella cranial base than seen in strepder to move the condyles closer to the center sirhines and colobines, respectively. The
of mass of the entire head, the posterior por- postural hypothesis also predicts that in intion of the cranial base is bent down and terspecific comparisons, animals that habitforward, while the anterior basicranium re- ually adopt more orthograde postures than
mains in its original orientation so that the their close relatives will exhibit more highly
eyes and face are maintained in a correct flexed basicrania.
forward-lookingplane (Fig. 1)(Wood Jones,
Facial-orientation hypothesis
1917; Weidenreich, 1924,1941).
It has long been speculated that facial poPostural uprightness alone does not appear to require a flexed basicraniurn, how- sition or orientation is in some way structurever. Birds, kangaroos, giraffes, camels, lla- ally associated with the form of the basicramas, and antelopes appear to have little nium (e.g., Virchow, 1857; Ranke, 1892;
trouble supporting extremely prognathic Cameron, 1924; Enlow, 1975, p. 203; Siriskulls on erect spines (Schultz, 1942) even anni and Swindler, 1979; p. 88).These specthough many of them have flat or lordotic ulations are indirectly supported by obserrather than ventrally flexed basicrania vations that the rate and timing of growth in
(Dabelow, 1929). Dabelow (1929) suggested the anterior cranial base appear to track
that ventral deflection of the face concomi- those of the masticatory apparatus (Ashton,
tant with postural uprightness should only 1957; Enlow, 1975).
The hypothesis regarding the structural
be expected to result in basicranial flexion
when the bony orbits are highly approxi- association between facial orientation and
mated to the midline and the roots of the the degree of basicranial flexion predicts
cranial base anteriorly. This presumably results in increased basicranial flexion (Moss,
1958; Aiello and Dean, 1990) as evidenced
by the more coronally oriented petrous temporal bones seen in both the “robust” australopithecines and Homo (Dean, 1988).
Dean posited that the trend towards an enlarged cerebellum in these hominids may be
associated with increased manual dexterity.
BASICRANIAL FLEXION IN PRIMATES
that the orientations of the lower and upper
parts of the face relative to the posterior cranial base should be positively correlated
with the orientation of the anterior basicranium relative to the same axis. Primates are
ideal for evaluating these hypotheses because various primate taxa, from the level of
the suborder to the subfamily, exhibit significant, taxon-specific differences in the orientation of the upper and lower parts of the
face, as well as in the degree of flexion of the
cranial base.
To estimate the reliability of the means
we utilized the formula in Box 9.13 of Sokal
and Rohlf (1981, p. 263). Using the mean of
the standard deviations reported in Table 1
as an estimate of the true standard deviation, at a significance level of 0.05 and infinite degrees of freedom, a sample size of 6 is
80% sure of detecting a difference of 7"-8"
between two means. While this sample size
does not, therefore, allow fine discrimination between any single pair of means, our
analysis is aimed at discerning patterns at
taxonomic levels higher than the species.
MATERIALS AND METHODS
Sample
To test these hypotheses, angular and linear measures were taken from lateral radiographs and combined with linear and volumetric measures from the same skulls for
which radiographs were available. The radiographs were originally collected by
M.J.R. for research on circumorbital morphology in primates but were deemed suitable for the present study because they were
taken to ensure that the midsagittal plane of
each skull (represented by prosthion, nasion, and basion) was parallel to the film
and the collimeter of the x-ray machine. In
this way parallactic distortion was minimized.
Radiographs of between one and six wildshot adult individuals of 68 species of primates were available, although typically six
(three males and three females) were used
(see Table 1 for sample sizes). The specimens are housed in the American Museum
of Natural History in New York, the National Museum of Natural History in Washington, D.C., the Field Museum of Natural
History in Chicago, the Museum of Comparative Zoology in Cambridge, and the British
Museum (Natural History), London.
The techniques for taking the linear and
angular measurements from the radiographs were tested by replicating each measurement five times on radiographs of six
individuals of Callicebus moloch. The null
hypothesis, that the values for the replicate
measurements taken from one individual
are the same, was tested and confirmed with
analysis of variance (ANOVA) (P < 0.05).
309
Measurements
Angular data
Angular data (the CBA, angle of facial kyphosis [AFK], and angle of orbital axis orientation [AOA]) were taken from lateral radiographs by tracing the lines defining the
angles onto acetate overlaying the radiograph and measuring the angles to the nearest degree with a goniometer and protractor.
CBA. Measurements of flexion of the cranial base are usually made from midline
structures exposed in hemisected skulls or
in lateral radiographs. Because this flexion
occurs primarily a t the three basicranial
synchondroses (sphenoethmoid, midsphenoidal, spheno-occipital) (see review in Sirianni and Swindler, 19791, flexion was measured in this study using lines that do not
cross these synchondroses. Although our
CBA therefore differs from the traditional
measure of the CBA, we prefer it because it
enables interspecific differences in the values for basicranial flexion to be localized to
specific synchondroses of the cranial base.
Our measurements (Fig. 2) were aimed at
capturing the relative orientations of the endocranial surfaces of the clivus ossis occipitalis (CO) and the planum sphenoideum
(PSI. Given the difficulties inherent in identifying craniometric landmarks on lateral
radiographs, we attempted to approximate
those planes that reflect the orientations of
these surfaces on dry skuls. The midline endocranial surface of the CO was represented
by a line from basion to the posterior edge of
the spheno-occipital synchondrosis. When
the spheno-occipital synchondrosis was not
310
C F ROSS AND M J RAVOSA
TABLE 1 Cranral-base angle, sample s m s , postural categories, and neural sample
Taxon
Strepsirhini
Daubentoniidae
Daubentonia madagascariensis
Indriidae
fndri indri
Auahi laniger
Propithecus uerreauxi
Lemuridae
Eulemur fuluus
Varecia uariegata
Hapalemur griseus
Lepilemuridae
k p i l e m u r mus6etinus
Cheirogaleidae
Cheirogaleus major
Microcebus murinus
Mirza coquereli
Phaner furcifer
Lorisidae
Loris tardigradus
Nycticebus coucang
Arctocebus calabarensis
Perodicticus potto
Galagidae
Otolemur crassicaudatus
Euoticus elegantulus
Haplorhini
Tarsiidae
Tarsius syrichta
Platyrrhini
Callitrichidae
Callithrix argentata
Cebuella pygmaea
Saguinus fuscicollis
Leontopithecus rosalia
Callimico goeldis
Atelinae
Alouatta belzebul
Alouatta palliata
Ateles fusciceps
Ateles geoffroyi
Brachyteles arachnoides
Lagothrix lagothricha
Pitheciinae
Pithecia pithecia
Chiropotes satanas
Cacajao caluus
Cebidae
Cebinae
Cebus apella
Cebus capucinus
Saimiri sciureus
Aotinae
Aotus triuirgatus
Callicebus moloch
Catarrhini
Cercopithecoidea
Cercopithecinae
Cercopithecus aethiops
Cercopithecus mona
Cercopithecus mitis
Miopithecus talapoin
Erythrocebus patas
Macaca nigra
Macaca syluana
Theropithecuspelada
CBA'
mean
CBA
standard
deviation
Sample
size"
Posture3
18
Neural
sample4
12
157
7.19
5
P
X
168
180
168
5.53
4.59
2.86
6
6
6
0
0
0
X
X
X
171
177
175
3.01
5.50
3.92
6
6
6
P
P
0
X
178
4.08
6
0
X
181
157
158
179
5.94
5.23
P
0
X
X
-
6
4
1
2
162
171
168
181
0.50
3.31
3.91
4.29
6
6
5
6
P
167
4.23
7.97
6
P
158
6
50
0
147
5.33
6
19
0
164
161
170
173
171
2.42
2.97
2.44
5.68
4.22
6
6
6
6
6
0
186
188
161
162
160
176
5.60
7.09
3.97
7.34
7.29
5.95
6
6
6
6
5
6
P
P
182
170
172
4.62
4 09
2.81
6
6
6
0
P
P
X
173
172
169
5.14
6.15
4.19
6
6
6
P
P
0
X
X
X
180
175
1 26
3.51
P
P
X
171
170
179
168
167
158
154
151
5.48
3.78
3.06
3.61
6.69
4.63
5 60
4.92
6
6
30
24
13
6
6
6
6
6
6
4
-
6
0
0
P
X
X
?
P
0
0
0
0
P
0
0
0
X
X
X
X
X
X
10
7
4
P
P
P
X
P
P
X
P
-
P
P
(continued)
311
BASICRANIAL FLEXION IN PRIMATES
TABLE 1. Cranial-base angle, sample sizes, postural categories, and neural sample (Continued)
Taxon
Lophocebus albigena
Cercocebus torquatus
Papio anubcs
Mandrillus sphinx
Mandrillus leucophaeus
Colobinae
Colobus guereza
Piliocolobus badius
Procolobus uerus
Presbytis cristata
Presbytis nielalophos
Presbytis rubicunda
Presbytas entellus
Nasalis laruatus
Pygathrrr nemaeus
Simzas concolor
Rhinopithecus roxeilana
Hominoidea
Hylobatidae
Hylobates muelleri
Hylobates lar
Symphalangus syndactylus
Pongdae
Pongo pygmaeus
Pan troglodytes
Gorilla gorilla
CBA'
mean
CBA
standard
deviation
163
172
154
144
160
2.13
5.89
5.83
5.32
161
155
157
166
154
152
147
157
144
161
150
4.59
3.93
6.39
2.43
3.76
5.17
5.89
3.78
3.64
4.27
3.97
-
Sample
size'
6
6
6
6
1
11
6
6
6
6
6
6
6
6
6
6
6
6
Posture3
P
P
P
P
P
Neural
sam~le~
X
X
3
P
P
P
P
P
P
P
P
P
X
X
X
P
P
3
160
153
167
8.60
6.19
6.83
6
6
6
X
135
152
148
6.46
5.32
1.64
6
6
X
6
X
'
Cranial-base angle.
'Sample sizes for angular, volumetric, and linear measures. Linear and volumetric measures were takeu from the same individuals for which
radiographs were available. Sample sizes at the species levels represent the number of individuals measured for each species. Sample sizes for
taxa above the species level refer to the number of species-means within that taxon.
3Postural categories (0,
orthograde; P, pronograde) assigned according to assumptions detailed in text. Categories are relative to other taxa in
same Family (Strepsirhini and Hominoidea) or Subfamily (Platyrrhini and Catarrhini) only (Column 1).
*Sample sizes for neural measures. Species for which Stephan et al. (1981)give data on neural variables are marked with an 'X".Sample sizes for
taxa above the species level represent the number of species within that taxon for which there are data on neural variables.
visible in the lateral radiographs, we fitted a
line by eye to the endocranial surface of the
midsagittal section of the cranial base posterior to dorsum sellae. We believe this
method to be reliable, because in those radiographs in which the spheno-occipital synchondrosis was present and visible, the line
segment from basion to the posterior edge of
dorsum sellae approximated the endocranial surface of the clivus. We recognize the
limitations of these radiographically derived
measures, and suggest that they may be unsuited for documenting distinctions within
species or ontogenetic series, or between
closely related species. We do feel however
that these measures are useful for documenting broad trends at higher taxonomic
levels, as concern us here.
The orientation of the pre-sella basicranium was estimated by measuring the orientation of the endocranial surface of the PS
(Fig. 2). The posterior point of the PS is de-
fined as the apex, or the superiormost midline point on the declivity above the sulcus
chiasmatis. Unlike tylion, sella, and the pituitary point, this point lies in the plane of
the endocranial surface of the sphenoid. We
operationally define the anterior border of
the PS as the apex, or superiormost point on
the sloping posterior surface of the pit in
which the cribriform plate is set. In strepsirhines, this corresponds to the posterior
edge of the cribriform plate, or prosphenion.
The inferior angle formed by the intersection of the plane of the CO and the plane of
the PS is CBA.As this angle decreases the
cranial base becomes more flexed and as the
angle increases it becomes less flexed. If the
angle measures greater than 180" then the
PS is retroflexed on the clivus.
In order to evaluate Dabelow's postural
hypothesis, as well as the facial orientation
hypothesis, facial orientation relative to the
clivus was quantified using two measures,
C.F. ROSS AND M.J. RAVOSA
312
A
ans
/v-
pns
B
PS
ba’
.
fn
Fig. 2. Diagrams illustrating points used (A) to define planes and angles used (B) in this study as
measured from lateral radiographs. CBA,cranial-base angle; AOA,angle of orbital axis orientation; AFK,
angle of facial kyphosis; ac, anterior border of CO;ans, anterior nasal spine; ap, anterior border of planum
sphenoideum; ba, basion; co, plane of clivus ossis occipitalis; fn, plane of floor of nasal fossa; oa, plane of
orbital axis; pns, posterior nasal spine; pp, pituitary point; pps, posterior edge of planum sphenoideum;
ps, planum sphenoideum
palate and orbit orientation, reflecting the
orientation of the lower and upper faces, respectively.
AFK. The orientation of the palate relative to the clivus is most consistently represented on lateral radiographs and duplicated across taxa if it is registered as “a line
connecting the tips of the anterior and posterior nasal spines (Starck, 1954). Where
there is no distinct anterior nasal spine, this
line is drawn tangent to the dorsal surface of
the midsagittal section of the pre-maxilla”
(Cartmill, 1970, p. 63). This plane will there-
fore be referred to as the floor of the nasal
fossa. The inferior angle formed by the intersection of the plane of the floor of the nasal
fossa and the plane of the clivus is referred
to as the AF’K, or klinorhynchy (Hofer,
1952). The smaller the AFK, the more kyphotic, ventrally flexed, or klinorhynch the
skull. The greater the angle the less kyphotic or more airorhynch (Hofer, 1952) the
skull.
AOA. The orientation of the orbital axis
was determined by the method outlined by
Ravosa (1988). The line of the orbital axis
BASICRANIAL FLEXION IN PRIMATES
was extrapolated anteriorly or posteriorly to
the plane of the clivus, and the inferior angle
between these two lines is defined as the
AOA.
Linear measures
Linear measures to the nearest tenth of a
millimeter were taken from both the radiographs (endocranial basicranial length [BL],
prosthion-palate length on the radiographs
[PBR]) and the original skulls (prosthionbasion length [PLI, prosthion-basion length
on the original skulls [PBSI) using dial and
digital calipers.
BL. In order to evaluate hypotheses that
measures of brain size relative to BL are
important determinants of the degree of basicranial flexion, the length of the endocranial surface of the basicranium was measured from the lateral radiographs. Three
segments were measured directly from the
radiographs: the distances between a) basion and pituitary point; b) pituitary point
and the posterior point on the PS (as defined
above); and c) the posterior and anterior
points of the PS. For each individual, a), b),
and c) were then summed and this value
converted into an estimate of “actual” BL by
multiplying it by PBSPBR.
PBR and PBS. Prosthion-basion length
on each radiograph (PBR) and on the original skulls (PBS) were measured to calculate
the correction factor (PBSPBR) used in calculating BL.
PL. The prosthion-staphylion distance
was measured to serve as a measure of the
size of the masticatory apparatus.
Volumetric measures
Neurocranial volume. Gould’s spatialpacking hypothesis suggests that overall
brain size relative to BL is the prime determinant of the degree of basicranial flexion.
Estimates of overall brain size were obtained by measuring the volume of the
braincase. The neurocranium was filled
with barley through the foramen magnum
while shaking it gently from side to side,
then it was tapped several times firmly on
the side with a finger and filled again. This
procedure was repeated until no more barley would fit inside the level of the foramen
magnum. The barley in the braincase was
then emptied into a graduated cylinder
313
which was shaken until the barley was
packed down and formed a level surface at
the top. The volume was then read off the
graduated cylinder to the nearest ml.
Neocortex, telencephalon, and cerebellum volume. The neocortex appears to have
increased with positive allometry relative to
overall brain size in primate evolution
(Passingham, 1975), suggesting that increasing neocortex size relative to BL may
be an appropriate measure of relative encephalization. The size of the cerebral hemispheres may also be appropriate-the cerebrum, or telencephalon, includes not only
the neocortex, but also its thalamocortical
and corticocortical connections, in addition
to the archicortex and paleocortex, with
their underlying medullary substance or
white matter, the basal ganglia, and the lateral ventricle. Thus, the cerebrum represents a morphological level that is intermediate between that of the neocortex and the
entire brain. Data on the volume of the neocortex, telencephalon, and cerebellum in 35
of these species were taken from Stephan et
al. (1981).
Postural behavior
Data on postural behavior were taken
from the literature (Fleagle, 1977, 1988;
Mittermeier, 1978; Fleagle and Mittermeier, 1980; Hunt, 1991). This required two
assumptions: first, that animals which leap
more also have more orthograde body postures than nonleaping close relatives; and
second, that animals with more orthograde
body postures also have more orthograde
head postures. While acknowledging that
these assumptions may be too broad, the relevant data with which to evaluate them are
lacking. Broad qualitative distinctions were
made between those animals that are often
in fairly orthograde postures (sitting, standing, clinging vertically, brachiating) and
those that tend to be more pronograde (quadrupedalism, both terrestrial and arboreal).
Statistical analyses
To test for sexual dimorphism in the CBA,
the angle was measured on radiographs of
six male and six female Macaca fascicularis
and an ANOVA (P < 0.05) used to test for
significant differences associated with sex.
In Macaca the CBA showed no significant
314
C.F. ROSS AND M.J. RAVOSA
added variance component associated with
sex. While this does not indicate the absence
of sexual dimorphism in the CBA in other
taxa, the absence of such dimorphism in a
taxon with such extreme body-size dimorphism imples that this may be the case. Consequently, combined-sex species means
were used for all analyses.
Evaluating Gould’s Spatial-Packing hypothesis involves testing for significant correlations between the size of the CBA and
the volume of the neurocranium, neocortex
and telencephalon relative to BL. To do this,
the ratio of the cube root of each of these
neural measures to BL was calculated. The
null hypothesis, that there is no skewness in
the distributions of these ratios, was tested
using formulae in Boxes 7.1 and 7.4 of Sokal
and Rohlf (1981: 139 & 174) and confirmed
at P < 0.001. The cube root of neurocranial
volume/BL constitutes Index of Relative Encephalization 1(IRE1); cube root neocortical
volume/BL is IRE2; and cube root telencephalon volume/BL is IRES.
To evaluate Biegert’s Spatial-Packing hypothesis that a large neocortex relative to
the size of the masticatory apparatus is correlated with a decrease in the CBA, the ratio
of the cube root of neocortical volume/palate
length (IRE 4) was calculated and tested for
skewness (null hypothesis of no skewness
was confirmed at P < 0.001).
The hypotheses outlined in the introduction were then evaluated by computing
Pearson correlations (P < 0.05, see Table 3)
for bivariate comparisons between the CBA
and the following variables:
1.IREs 1,2, and 3 (Gould’s Spatial-Packing hypothesis); 2. IRE 4 (Biegert’s SpatialPacking hypothesis); 3. cerebellum volume
(Cerebellum Hypothesis) (log, and raw
CBA); 4. AOA (Postural Hypothesis and
Facial-Orientation Hypothesis) (raw variables); and 5. the AFK (Facial-Orientation
Hypothesis) (raw variables). These comparisons were performed at the level of the Order (all Primates), Suborder (Haplorhini
and Strepsirhini), Infraorder (Platyrrhini
and Catarrhini), Superfamily (Hominoidea,
Cercopithecoidea) and Subfamily (Cercopithecinae, Colobinae).
Partial correlation analyses (P < 0.05)
were carried out in order to isolate that proportion of the total variance in the CBA
associated with one independent variable
while controlling for a correlation with another independent variable. These partial
correlation analyses were performed using
the natural logs of all variables to enable the
angular and cerebellum volume data to be
compared with the IREs.
Postural data, consisting of categorical or
discrete variables, were compared with values for the CBA using a non-parametric
Mann-Whitney U-Test (Sokal and Rohlf,
1981).
RESULTS
Neural theories
Bivariate comparisons of IRE1 and the
CBA reveal a highly significant negative
correlation across primates (r = -0.6451,
haplorhines ( - 0.684), platyrrhines (-0.504)
and catarrhines (-0.537) (Fig. 3, Table 2).
No significant relationship was revealed for
strepsirhines. Within catarrhines, significant correlations were observed across
colobines (-0.687). Among hominoids, although r = -0.790, the correlation was not
significant. These results provide support
for Gould’s hypothesis that a large brain
relative to basicranial length should be associated with increased basicranial flexion,
at least at higher taxonomic levels within
haplorhines.
Comparisons of IRE2 and IRE3 with values for the CBA reveal significant negative
relationships across primates as a whole
(IRE2 = -0.540; IRE3 = -0.6061, and haplorhines (IRE2 = -0.567; IRE3 = -0.619).
Catarrhines (- 0.640) and cercopithecoids
(-0.769) also show significant negative correlations between IRE3 and the CBA. Strepsirhines do not show a significant relation.
It is interesting to note that, although these
relationships were not significant, IREs 2
and 3 were negatively related to the cranial
base angle in hominoids and cercopithecines
(with high “r”s),but positively related in
colobines. The negative correlations indicate
that as neocortex and cerebrum size relative
to basicranial length increase across all primates, the CBA decreases. This provides
only weak corroboration for hypotheses that
the sizes of the neocortex and cerebrum relative to basicranial length are associated
with increased basicranial flexion. The
BASICRANIAL FLEXION IN PRIMATES
315
Tarsius
CALL I T R l C H l D A E
ATELINAE
PlTHECllNAE
CEBIDAE
CERCOPITHECINAE
COLOBINAE
HYLOBAT I DAE
PONGIDAE
IRE1
Fig. 3. Plot of the angle of basicranial flexion vs. IRE 1 (ratio of cube root of neurocranial volume to
basicranial length) in haplorhine primates.
TABLE 2. Correlation coefficients for biuariate cornparisom evaluating hypotheses
Cranial-base angle (CBA) vs
CBA raw (R) or log, (L)
Primates
Strepsirhini
Haplorhini
Platyrrhini
Catarrhini
Hominoidea
Cercopithecoidea
Cercopithecinae
Colobinae
IRE1
IRES
IRE3
IRE4
R & (L)
R
R
R
Cerebellum volume
rawhog,
W(L)
-0.606***
-0.32911s
-0.619**
0.23111s
-0.640*
-0.49011s
-0.769*
-0.909ns
0.419ns
0.0720ns
-0.205ns
0.35511s
-0.624*
-0.038ns
0.920ns
-0.13311s
0.83411s
-0.769ns
-0.466**/-0.300ns
-0.318nd0.022ns
-0.464*/-0.286ns
0.011ns/0.314ns
-0.455nd-0.517ns
-0.940nd-0.84911s
-0.343nd-0.36411s
-0.917nd-0.968*
0.720nd0.735ns
-0.540**
-0.32911s
-0.567**
-0.lOlns
-0.504*
-0.537**
-0.59711s
-0.50911s
-0.79011s
-0.335ns(L) -0.70711s
0.203ns(L) -0.92911s
0.603ns
-0.687*
-0.645***
-0.36011s
-0.684***
AOA
AFK
R
R
0.608***
0.469***
0.379ns
0.42211s
0.617***
0.429***
0.723***
0.465*
0.34611s
-0.03311s
0.443ns
0.054ns
0.746***
0.232ns
0.853***
0.746***
0.784**
0.36011s
IREl, ratio ofcube root of neurocranial volume to BL; IRE2 ratio of cube root of neocortical volume to BL; IRE3 ratio of cube root of telencephalon
volume to BL, IRE4 ratio of cube root of neocortical volume to P L AOA, angle of orbital axis orientation; AFK, angle of facial kyphosis. All
analyses were performed using raw values, except where noted with (L) h e . , Cerebellum volume vs CBA and two comparisons of CBA and IRE1).
* P i 0.05;**P< 0.01; ***P < 0.001; ns = P > 0.05.
break-down of these relationships within
hominoids may be attributable to low sample sizes. The lack of a significant correlation between IRE2 and CBA across cercopithecoids is due to the presence of opposing
trends within the constituent subfamilies.
Biegert’s Spatial-Packing hypothesis predicts that the CBA should be positively correlated with increasing palate length (i.e.,
the angle should get larger and the basicranium less flexed). Bivariate comparisons reveal that across all primates, haplorhines,
catarrhines, and cercopithecines the CBA
actually decreases, and the basicranium becomes more flexed, as palate length increases (Fig. 4, Table 3). Bivariate comparisons provide some support for Biegert’s
suggestion that increasing neocortical volume should be associated with a decreasing
CBA, the predicted relationship being seen
across primates and haplorhines as a whole,
but only when raw data are used (Table 3).
Biegert’s Spatial-Packing hypothesis also
predicts that increasing neocortex size relative to the size of the masticatory apparatus
will be negatively correlated with the CBA.
Across primates the correlation between
neocortical volume and palate length is significant and negatively allometric (r =
0.889; slope = 2.45). Bivariate comparisons
reveal the ratio of neocortical volume to
palate length (IRE 4) and the CBA to be
significantly negatively related only among
platyrrhines (-0.624). These results provide
C.F. ROSS AND M.J. RAVOSA
316
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Fig. 4. Plot of the angle of basicranial flexion vs. palate length (loge)in haplorhine primates. Relation
ship across strepsirhines is not significant. See Table 2 and text.
only very limited support for Biegert’s hypothesis that a large masticatory apparatus
relative to neocortical volume is associated
with increased basicranial flexion.
Aiello and Dean (1990) suggest that increasing cerebellum size may serve to deflect the posterior portion of the cranial base
anteriorly, resulting in greater basicranial
flexion. Comparisons between log-transformed values for the CBA and cerebellum
size reveal no significant relationship for
any taxonomic group save cercopithecines
(-0.968) (Table 2). Using raw values, cerebellum volume is negatively correlated with
the CBA across primates (-0.466) and haplorhines (-0.464), providing some support
for the Cerebellum Hypothesis. Among
homninoids, the correlation coefficients for
this bivariate comparison are high but not
significant, suggesting that increased sample size might confirm this hypothesis in
this group.
Postural Hypothesis
Dabelow’s hypothesis, that increased flexion is associated with ventral deflection of
the face when the orbits are highly approximated in the midline, is corroborated. As
predicted, there is a significant positive relationship between the CBA (the orientation
of the pre-sella relative to the post-sella cra-
nial base) and the orientation of the orbits
relative to the post-sella cranial base among
haplorhines (0.6171, but not among strepsirhines (Table 2; Figure 5). Platyrrhines
also show a positive correlation between
basicranial flexion and orbit orientation
(0.723). This relationship is not found
among catarrhines overall, but it is found in
cercopithecoids (0.7461, cercopithecines
(0.853) and colobines (0.784). Moreover, as
predicted, cercopithecines show a higher
r-value than is seen in colobines, indicating
that there is a closer correlation between the
angle of flexion and orbit orientation in the
former than the latter.
Demonstration of a relationship between
basicranial flexion and orbit orientation
corroborates Dabelow’s hypothesis, but it
does not necessarily support the prediction
of the postural hypothesis that basicranial
flexion should be associated with orthograde head and body postures. MannWhitney U-Tests within families and subfamilies revealed that atelins (i.e., Ateles,
Brachyteles, Lagothrix) are the only taxa
which utilize orthograde body postures (suspension) and exhibit more flexed basicrania
than closely related forms with more pronograde habits (i.e., Alouatta). This result
does not provide strong support for the postural hypothesis.
not significant,P > 0.05
-0.473**/0.300ns
-0.326ns/-O.O12ns
-0.471*/-0.257ns
- 0.005ns/- 0.301ns
-0.424nsi-0.404ns
-0.802ns/-0.747ns
-0.154ns/-O.O91ns
-0.890ns/-0.938ns
0.726ns/0.734ns
-0,514**"/-0,387***
-0.026ns/-O.l93ns
-0.507***/-0.389**
-0.167ns/-O.O94ns
-0.503**/-0.543***
-0.694nd-0.68311s
-0.335nd-0.375*
-0.722***/-0.726***
-0.576*/-0.589*
-0.334**/-0.254*
0.234nd-0.30411s
-0.321*/-0.236ns
0.330nd0.354ns
-0.416*/-0.410*
-0.613ns/-0.600ns
-0.186ns/- 0.190ns
-0.615*/-0.602*
0.155nd0.142ns
-0.415***/-0.363**
0.227nd0.273ns
-0.423***/-0.384"*
0.293nd0.304ns
-0.320*/-0.295ns
-0.625ns/-0.588ns
-0.156ns/-O.l34ns
-0.706***/-0.716***
0.011ns/O.O06ns
=
Neocortical volume
rawflog, (XI
Neurocranial volume
rawflog, (XI
Basicranial length
rawflog, (XI
Palate length
raw/log, (XI
* P < 0 05; **P < 0.01: ***P < 0,001; ns
Primates
Strepsirhini
Haplorhini
Platyrrhini
Catarrhini
Hominoidea
Cercopithecoidea
Cercopithecinae
Colobinae
Cranial-base angle vs.
TABLE 3. Correlation coefficients for bivariate comparisons between the cranial-base angle and linear and neural variables
-0.506"*/-0.381*
-0.327ns/-O.O06ns
-0.494*/-0.342ns
0.772*/0.828*
-0.428nd-0.415ns
-0.809nd-0.75311s
-0.169nd-0.114ns
- 0.890nd- 0.939ns
0.700ndO.705ns
Telencephalon volume
raw/log, (XI
C.F. ROSS AND M.J. RAVOSA
318
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155 160 165 170 175 180 185
ORBITAL AXIS ORIENTATION (DEGREES)
190
195
Fig. 5. Plot of raw values of the angle of basicranial flexion vs. the angle of orbital axis orientation in
haplorhine primates. Relationship across strepsirhines is not significant. See Table 3 and text.
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Fig, 6. Plot of raw values of the angle of basicranial flexion vs. the angle of facial kyphosis in haplorhine
primates. Relationship across strepsirhines is not significant. See Table 3 and text.
Facial-orientation hypothesis
Partial correlation models
The orientation of the palate is significantly positively correlated with the CBA at
the ordinal level (0.469) (Table 2, Fig. 6). At
the subordinal level only haplorhines show a
significant relationship (0.422) and, within
haplorhines, platyrrhines (0.465)and cercopithecines (0.746)show this relationship but
catarrhines as a whole do not.
All independent variables found to be significantly correlated with the CBA in bivariate comparisons were included in partial
correlation models evaluated at all taxonomic levels within haplorhines (where necessary). Because none of the variables considered here were significantly correlated
with the CBA across strepsirhines and
BASICRANIAL FLEXION IN PRIMATES
among hominoids, partial correlation models were not tested within these taxa. Similarly, across catarrhines only IRE 1is significantly related to the CBA, so partial
correlation analyses were not performed.
(Partial correlation models incorporating interaction terms were not significant at any
taxonomic level, so multiple regressions
were not required.)
Partial correlations between the CBA and
both palate orientation and orbit orientation
at all taxonomic levels within haplorhines
revealed that, independent of orbital axis
orientation, palate orientation accounts for
none of the variation in the CBA. These results provide no support for the assertion
that palate orientation is an important determinant of the CBA.
Across primates (0.7321, haplorhines
(0.816), and among colobines (0.940) the
most parsimonious partial correlation
model (i.e., the one with the highest correlation coefficient and significant independent
variables) includes the angle of orbital axis
orientation (positively correlated) and IRE 1
(negatively correlated). Across platyrrhines
neuriocranial volume relative to basicranial
length explains none of the variance in the
cranial base angle when the angle of the orbital axis is taken into account. For catarrhines and cercopithecoids, the best model
included only telencephalon volume relative
to basicranial length (IRE 3), which is negatively correlated with the CBA. Across cercopithecines only the AOA is included in the
most parsimonious model explaining variance in the CBA.
DISCUSSION
Neural hypotheses
Gould (1977) suggested that brain size
relative to BL is a more important cause of
the degree of basicranial flexion than brain
size relative to other (unspecified) measures. As predicted by this hypothesis, at
several taxonomic levels within haplorhines
an increase in overall brain size relative to
the length of the basicranium is associated
with an increase in basicranial flexion, although it remains to be determined whether
this association reflects a causal connection
between these variables. Regardless, flexion
319
effectively increases neurocranial volume
without increasing BL, in a fashion analogous to increasing the proportion of a sphere
which is utilized without increasing the
sphere’s diameter.
Gould’s spatial-packing hypothesis is supported by observations that juvenile primates tend to have larger brains relative to
body and skull size than their adult stages
(Gould, 19751, as well as having more flexed
basicrania. Nonhuman primate cranial ontogeny is characterized by a decrease in both
relative brain size and the degree of flexion,
whereas in human ontogeny the relatively
large brain and flexed basicranium seen in
the juvenile are retained into adulthood
(Ashton and Zuckerman, 1952, 1956; Zuckerman, 1955; Schultz, 1955; Ford, 1956;
Moore et al., 1973;Adams and Moore, 1975).
As an explanation for extreme basicranial
flexion in humans, Gould’s spatial-packing
hypothesis is supported by observations
that the human cranial base is “anteroposteriorly compressed relative to that of other
extant hominoids due to “both a reduction in
the length of the sphenoid bone” and “the
forward displacement of the foramen magnum and occipital condyles” (Dean and
Wood, 1984, p. 70). Cross-sectional data on
basicranial growth in extant hominoids suggest that these “shorter lengths of the human cranial base . . . result from a reduction
in the early postnatal spurt and an early
cessation of growth that continues in the
apes after growth has ceased in Homo sapiens” (Dean and Wood, 1984, p. 176). The
comparative data presented here provide
some corroboration for Gould’s spatial-packing hypothesis, but data on human basicranial flexion are required to confirm it,
This study found little evidence to suggest
that variation in neocortex or volume relative to BL accounts for variation in the CBA
in haplorhines. There is more evidence t o
suggest that telencephalon volume relative
to BL is an important determinant of the
CBA in catarrhines. That there was not
greater concordance between the results for
the different IRES is surprising, considering
that relative neurocranial volume is correlated with the degree of flexion, and that
anthropoids have more neocortex and telencepahlon relative to brain size than prosimi-
320
C.F. ROSS AND M.J. RAVOSA
ans (Passingham, 1975, 1982). This may be facial orientation explains the extreme dedue to the fact that anthropoids exhibit “a gree of basicranial flexion in humans, then
larger increase in gyrification for every unit why do lagomorphs and orangutans apparincrease in body or brain weight or neopal- ently reorient their face without modifying
lial volume” than prosimians (Zilles et al., the cranial base?
Dabelow argued that a shift to an or1989, p. 143). Whereas brain weight and volume are the best predictors of neocortical thograde posture should only result in ingyrification among prosimians, neocortical creased basicranial flexion, in association
volume is more important among anthro- with ventral deflection of the face, in those
poids. Thus, increases in neocortical volume animals with highly approximated bony orin anthropoids may be accompanied by in- bits. Dabelow’s hypothesis predicts a close
creases in gyrification, rather than in- correspondence between orbital axis oriencreased neurocranial volume and increased tation and the CBA in haplorhines but not in
strepsirhines, haplorhines in general havflexion of the cranial base.
There is only limited evidence at present ing narrower interorbital regions relative to
to support the contention of Aiello and Dean skull length than strepsirhines. This predic(1990) and Moss (1958) that increased cere- tion is supported. In strepsirhines with
bellum size is a major cause of increased highly approximated bony orbits, like Loris
basicranial flexion. Biegert’s (1963) sugges- tardigradus, the narrowest interorbital distion that the degree of flexion is determined tance lies above the olfactory tract, not beby the size of the neocortex relative to the low it, as in haplorhines (Cartmill, 1972).In
masticatory apparatus is also not corrobo- strepsirhines, therefore, the orientation of
the anterior limb of the basicranium need not
rated.
covary with orbital axis orientation as the
Postural hypothesis
medial orbital walls are not closely applied
The hypothesis that postural uprightness to the basicranium. Similarly, because they
alone necessitates a flexed basicranium is have a narrower interorbital distance, cercorefuted by cases where reorientation of the pithecines show a closer correlation between
face appears to have occurred without re- orbital axis orientation and the CBA than
quiring correlated changes in the orienta- colobines, as well as showing a correlation
tion of the anterior part of the cranial base. between CBA and AFK not seen in colobines.
Although orbit orientation is correlated
Ventral flexion of the face relative to the
braincase in posturally upright lagomorphs with the degree of basicranial flexion in hapis not associated with flexion of the cranial lorhines, it remains to be determined
base (DuBrul, 1950; Plate 2). Within Old whether differences in either of these craWorld monkeys, colobines have more dor- nial angular values are determined by possally deflected (airorhynch) faces than cer- tural differences. The postural hypothesis
copithecines, although they have similar de- asserts that phylogenetic changes in body
grees of basicranial flexion (Ravosa and orientation require alterations in visual axis
Shea, 1993). Similarly, the orangutan, orientation in order to maintain the eyes in
Pongo, has an extremely airorhynch face the forward-facing plane. These alterations
(i.e., dorsally deflected) relative to the Afri- are presumably achieved by changing the
can hominoids Pan and Gorilla, but it has orientation of both the bony orbits and the
much greater flexion of the cranial base. pre-sella basicranium relative to the postThat the face has rotated up and backwards sella cranial base, thus resulting in changes
relative to the basicranium in Pongo is in- in the degree of basicranial flexion, either as
dicated by several features of the anterior an essential part of the reorientation of the
cranial fossa, such as stenosis or pinching of bony orbits (Wood Jones, 1917) or as a pleiothe nasofrontal ethmoidal area (Montagu, tropic effect (Dabelow, 1929).
This hypothesis explains the condition in
19431, reduction of the sphenoidal sinuses
(Cave and Haines, 1940) and the cribriform posturally upright lagomorphs and kangaplate, and an increased frequency of meseth- roos, which have their orbits well separated
moid-presphenoid articulation (Montagu, in the midline, but it does not explain the
1943) (reviewed in Shea, 1985, p. 336). If situation in Pongo. Pongo has a narrow in-
BASICRANIAL FLEXION IN PRIMATES
terorbital region when compared to the African apes and Homo, in combination with an
airorhynch face and a highly flexed basicranium. Nor does it make sense of the situation in birds. Dabelow’s postural hypothesis
only makes sense if the orbital approximation in birds and Pongo occurred after reorientation of the face in phylogeny, or if it
follows the establishment of spatial relationships between the neurocranium and
splanchnocranium during ontogeny.
The most serious objection to the postural
hypothesis is that most mammals, and certainly primates, have flexible necks which
enable them to reorient their visual axes in
the frontal plane by flexing and extending
the whole head. Assuming that this option is
indeed available to all primates, is natural
selection likely to alter circumorbital morphology, resulting in profound reorganization of the neurocranialhplanchnocranial
boundary and the olfactory, respiratory, and
masticatory systems? The answer to this
question must await the gathering of data
on head posture and visual axis orientation
relative to the neck and trunk in living primates. Meanwhile, although we have supported Dabelow’s prediction that orbital orientation and basicranial flexion should be
correlated in animals with highly approximated bony orbits, the only taxon in which
we found a significant relationship between
posture and the degree of flexion was atelines. Atelines also exhibit a significant negative relationship between IRE1 and the
CBA (r = -0.887; p = .045) however, suggesting that relative brain size may be determining flexion in these animals. In any
event, the postural hypothesis does not provide a general explanation for basicranial
flexion among primates.
Facial orientation
These comments notwithstanding, the observed correlation between orbit orientation
and basicranial flexion in animals with
highly approximated orbits does imply that
facial orientation may be affected by basicranial morphology. Although palate and orbit orientation are significantly correlated
with each other across all primates (Ravosa,
1991) and both are significantly correlated
with the CBA across Haplorhini, the partial
correlation analyses indicate that palate ori-
321
entation explains none of the variation in
the CBA when orbital axis orientation is
taken into account.
Partial independence in the orientation of
upper and lower facial skeletons is also indicated by Ravosa’s (1988, 1991) work on
browridge morphology in primates. Ravosa
found that among cercopithecoidsthe orientation of the orbital axis relative to the basicranium is significantly correlated with
anteroposterior dimensions of the supraorbital torus. This indicates that anteroventral rotation of the orbital margins results in
increased disjunction between neural and
orbital cavities, necessitating the development of a supraorbital torus to roof the orbits. Ventral deflection of the palate, however, is not correlated with anteroposterior
browridge dimensions in any primates, even
though it is correlated with orbital axis orientation. Ravosa’s results, and those reported here, suggest that the significant correlations observed in bivariate comparisons
between palate orientation and the CBA are
merely due to palate orientation tracking orbital axis orientation.
In addition to showing covariance of orbital axis orientation and the CBA, extant
anthropoids also share the rare combination
of highly frontated and convergent bony orbits (Cartmill, 1970). In most animals the
degree of orbital convergence, or the extent
to which the two orbital axes are parallel,
varies inversely with orbital frontation (or
the degree of verticality of the orbits). This is
not the case in haplorhines. Tarsiers and
anthropoids not only have relatively parallel
orbital axes, but they also have more vertically oriented orbital rims than strepsirhines. This morphological combination
brings the medial walls of the orbital cones
into close approximation, forming, in small
haplorhines, an apical interorbital septum
situated immediately ventral to the cribriform plate and the anterior limb of the basicranium. It is probably as a direct result of
this structural integration of the medial orbital wall and the pre-sella basicranium
that the orientations of the orbital axes and
the anterior limb of the basicranium are
found to covary in interspecific comparisons
among haplorhines.
It remains to be determined why haplorhines combine greater orbital conver-
322
C.F. ROSS AND M.J. RAVOSA
gence with greater orbital frontation. Cartmill (1970) noted that a positive correlation
between the degree of orbital frontation and
convergence is also seen in indriids. Indriids
share with haplorhines the possession of relatively broad frontal lobes (Radinsky, 1968),
and Cartmill suggested that at least some of
the frontation seen in anthropoids may be
due to an anterior expansion of the neocortex pushing the superior orbital margin forward, expansion which could also cause ventral deflection of the orbital axes.
However, as Cartmill himself pointed out,
this does not explain the situation in large
anthropoids, like cercopithecoids and hominoids, which, due to the negative allometry
of brain on body size, have relatively small
brains for their body size, yet maintain
highly frontated orbits in spite of the fact
that the resulting disjunction between neural and orbital cavities must be bridged with
bone (Ravosa, 1988, 1991). If increased
brain size relative to BL influences basicranial flexion, and in turn, ventral deflection
of the orbital axes, why does the brain not
expand out over the orbits, utilizing the
space that its own expansion creates?
This may be due to increase in the size of
parts of the brain that do not lie over the
orbits, such as the occipital, parietal, and
temporal lobes, or the cerebellum. Partial
correlation analyses across haplorhines and
colobines certainly indicate that increasing
overall brain size (as measured by total neurocranial volume) has an effect on the CBA
independent of orbital axis orientation.
CONCLUSIONS
Although this study of the correlates of
basicranial flexion perhaps raises as many
questions as it answers, it does provide new
insights into the changes in craniofacial
morphology occurring at the origins of anthropoids and humans. The last common ancestor of all anthropoids, and maybe the last
common ancestor of anthropoids and extant
tarsiers, appears to have had a combination
of features that can be claimed to constitute
a new Bauplan. Most important for subsequent changes in anthropoid craniofacial
morphology was the approximation of the
bony orbits in the midline, creating strutural interdependence between the anterior
cranial base and fossa, and the underlying
orbital cavities. Large brain size relative to
BL, possibly due to an increase in the size of
the neocortex of the temporal and occipital
lobes, was associated with increased flexion
of the cranial base and associated ventral
deflection of the orbital axes and upper face.
Determination of whether these traits are
synapomorphies of a clade containing only
anthropoids and tarsiers, synapomorphies
of a broader haplorhine clade sensu (Szalay
et al., 19871, or convergences (Simons and
Rasmussen, 1989, Rasmussen, 1990) must
await the discovery of more fossils. Certainly, these modifications in the spatial relationships between the orbits and the neurocranium provided room for expansion of
the frontal lobes in later evolutionary lineages.
Gould’s spatial-packing hypothesis as an
explanation for the extreme basicranial
flexion seen in humans is supported by the
comparative evidence presented here. Corroboration with the comparative method is
the most powerful means of rendering putative human “uniquenesses”nonunique, and
therefore intelligible. Human uniquenesses
are not explicable, exactly because they are
unique (Cartmill, 1990). However, many
morphological features believed to be
unique to humans, basicranial flexion for
example, are explicable because they are not
unique in themselves, but represent extreme instantations of rules and principles
that underlie the generation of form across
primate taxa. Because demonstration of
that nonuniqueness involves comparisons
with other animals, such morphological features can only be explained by using the
comparative method.
The comparative data provide little support for the idea that orthograde head and
body postures require a flexed basicranium,
although confirmation of this must await
more detailed information on postural behavior in living primates. We suggest that
the high degree of basicranial flexion in humans can be explained as an extreme instance of a general rule that large brains
relative to BL tend to be associated with increased basicranial flexion.
ACKNOWLEDGMENTS
C.F.R. thanks Dr. John Carmen, Department of Anatomy, Auckland Medical School,
BASICRANIAL FLEXION IN PRIMATES
Auckland, New Zealand, for his enthusiastic
support at the inception of this project. The
authors also thank Drs. Matt Cartmill and
Bernard Wood, as well as two anonymous
reviewers, for helpful comments on a n earlier draft of this paper. The authors greatly
appreciate the timely comments of Dr. Bill
Jungers. This research was supported by
grants to C.F.R. from the National Science
Foundation (BNS-9100523) and the Duke
University Graduate School, and grants to
M.J.R. from the National Science Foundation (BNS-8813220), the National Institutes
of Health (DE055951, Northwestern University (0100-510-110Y),and the American
Museum of Natural History. Both C.F.R.
and M.J.R. were also supported by the Department of Biological Anthropology and
Anatomy, Duke University Medical Center.
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