The primate cranial base: ontogeny, function and - Harvard University
The primate cranial base: ontogeny, function and - Harvard University
The primate cranial base: ontogeny, function and - Harvard University
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YEARBOOK OF PHYSICAL ANTHROPOLOGY 43:117–169 (2000)<br />
<strong>The</strong> Primate Cranial Base:<br />
Ontogeny, Function, <strong>and</strong> Integration<br />
DANIEL E. LIEBERMAN, 1 CALLUM F. ROSS, 2 AND MATTHEW J. RAVOSA 3<br />
1 Department of Anthropology, George Washington <strong>University</strong>,<br />
Washington, DC 20052, <strong>and</strong> Human Origins Program, National Museum<br />
of Natural History, Smithsonian Institution, Washington, DC 20560<br />
2 Department of Anatomical Sciences, Health Sciences Center, SUNY at<br />
Stony Brook, Stony Brook, NY 11794-8081<br />
3 Department of Cell <strong>and</strong> Molecular Biology, Northwestern <strong>University</strong><br />
Medical School, Chicago, Illinois 60611-3008, <strong>and</strong> Mammals Division,<br />
Department of Zoology, Field Museum of Natural History,<br />
Chicago, Illinois 60605-2496<br />
<strong>cranial</strong> <strong>base</strong>; basicranium; chondrocranium; pri-<br />
KEY WORDS<br />
mates; humans<br />
ABSTRACT Underst<strong>and</strong>ing the complexities of <strong>cranial</strong> <strong>base</strong> development,<br />
<strong>function</strong>, <strong>and</strong> architecture is important for testing hypotheses about<br />
many aspects of craniofacial variation <strong>and</strong> evolution. We summarize key<br />
aspects of <strong>cranial</strong> <strong>base</strong> growth <strong>and</strong> development in <strong>primate</strong>s that are useful<br />
for formulating <strong>and</strong> testing hypotheses about the roles of the chondrocranium<br />
<strong>and</strong> basicranium in <strong>cranial</strong> growth, integration, <strong>and</strong> <strong>function</strong> in <strong>primate</strong> <strong>and</strong><br />
human evolution. We review interspecific, experimental, <strong>and</strong> ontogenetic<br />
evidence for interactions between the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> brain, <strong>and</strong> between<br />
the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> the face. <strong>The</strong>se interactions indicate that the <strong>cranial</strong><br />
<strong>base</strong> plays a key role in craniofacial growth, helping to integrate, spatially<br />
<strong>and</strong> <strong>function</strong>ally, different patterns of growth in various adjoining regions of<br />
the skull such as components of the brain, the eyes, the nasal cavity, the oral<br />
cavity, <strong>and</strong> the pharynx. Brain size relative to <strong>cranial</strong> <strong>base</strong> length appears to<br />
be the dominant influence on many aspects of basi<strong>cranial</strong> variation, especially<br />
the angle of the <strong>cranial</strong> <strong>base</strong> in the midsagittal plane, but other factors<br />
such as facial size, facial orientation, <strong>and</strong> posture may also be important.<br />
Major changes in <strong>cranial</strong> <strong>base</strong> shape appear to have played crucial roles in<br />
the evolution of early <strong>primate</strong>s, the origin of anthropoids, <strong>and</strong> the origin of<br />
Homo sapiens. Yrbk Phys Anthropol 43:117–169, 2000. © 2000 Wiley-Liss, Inc.<br />
TABLE OF CONTENTS<br />
Glossary, L<strong>and</strong>mark, <strong>and</strong> Measurement Definitions ....................................................... 118<br />
Introduction ......................................................................................................................... 120<br />
Anatomy <strong>and</strong> Development ................................................................................................ 120<br />
Development of the chondrocranium ............................................................................. 121<br />
Patterns <strong>and</strong> processes of basi<strong>cranial</strong> growth .............................................................. 122<br />
Antero-posterior growth .............................................................................................. 123<br />
Medio-lateral growth ................................................................................................... 125<br />
Supero-inferior growth ................................................................................................ 126<br />
Angulation .................................................................................................................... 126<br />
Associations Between Cranial Base <strong>and</strong> Brain ................................................................ 131<br />
Brain size <strong>and</strong> <strong>cranial</strong> <strong>base</strong> angle .................................................................................. 131<br />
Brain shape <strong>and</strong> <strong>cranial</strong> <strong>base</strong> angle .............................................................................. 134<br />
© 2000 WILEY-LISS, INC.
118 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Brain volume <strong>and</strong> posterior <strong>cranial</strong> fossa shape .......................................................... 138<br />
Associations Between Cranial Base <strong>and</strong> Face .................................................................. 138<br />
Anterior <strong>cranial</strong> fossa shape <strong>and</strong> upper facial growth ................................................. 138<br />
Middle <strong>cranial</strong> fossa shape <strong>and</strong> midfacial growth ........................................................ 140<br />
Basi<strong>cranial</strong> width <strong>and</strong> overall facial shape in humans ................................................ 144<br />
<strong>The</strong> Cranial Base <strong>and</strong> Posture ........................................................................................... 148<br />
Major Unresolved Issues of Cranial Base Variation in Primate Evolution ................... 151<br />
Primate origins, encephalization, <strong>and</strong> circumorbital form .......................................... 151<br />
Anthropoid origins <strong>and</strong> <strong>cranial</strong> <strong>base</strong>-face interactions ................................................. 152<br />
Variation in hominin <strong>cranial</strong> <strong>base</strong> angle ....................................................................... 153<br />
Cranial <strong>base</strong> flexion <strong>and</strong> vocal tract shape in hominins .............................................. 154<br />
Cranial <strong>base</strong> shape <strong>and</strong> facial projection in Homo ....................................................... 156<br />
Cranial <strong>base</strong> characters in phylogenetic analyses ........................................................ 158<br />
Conclusions .......................................................................................................................... 159<br />
What major factors generate variation in the <strong>cranial</strong> <strong>base</strong>? ....................................... 160<br />
What role does the <strong>cranial</strong> <strong>base</strong> play in craniofacial integration? .............................. 160<br />
Correlation ................................................................................................................... 161<br />
Constraint .................................................................................................................... 162<br />
Ontogenetic sequence .................................................................................................. 162<br />
Future research ............................................................................................................... 163<br />
Acknowledgments ............................................................................................................... 163<br />
Literature Cited .................................................................................................................. 163<br />
GLOSSARY<br />
Basioccipital clivus: midline “plane” of the<br />
posterior <strong>cranial</strong> <strong>base</strong> formed by the superior<br />
(endo<strong>cranial</strong>) aspects of the basioccipital<br />
<strong>and</strong> the posterior sphenoid.<br />
Brain stem: the ventral parts of the brain,<br />
excluding the telencephalon. Specifically, in<br />
this paper, the brain stem consists of the<br />
medulla oblongata <strong>and</strong> mesencephalon (<br />
optic tectum <strong>and</strong> tegmentum) of Stephan et<br />
al. (1981; see also Butler <strong>and</strong> Hodos, 1996).<br />
Chondrocranium: cartilaginous precursors<br />
to the basicranium.<br />
Constraint: a limitation or bias on processes<br />
<strong>and</strong>/or patterns of evolution, growth, form,<br />
<strong>and</strong> <strong>function</strong>.<br />
Cranial <strong>base</strong> angulation: a series of events<br />
by which bone or cartilage deposition in the<br />
midline <strong>cranial</strong> <strong>base</strong> changes the angle between<br />
intersecting prechordal (see below)<br />
<strong>and</strong> postchordal (see below) lines. This causes<br />
the inferior <strong>cranial</strong> <strong>base</strong> angle to become more<br />
acute (flexion) or more obtuse (extension).<br />
Displacement: a series of events by which<br />
an osseous region “moves” relative to another<br />
osseous region through bone deposition<br />
(primary displacement), or through<br />
bone deposition in an adjoining bone (secondary<br />
displacement).<br />
Drift: a series of events by which an osseous<br />
wall “moves” relative to another anatomical<br />
region through bone deposition on one surface<br />
<strong>and</strong> bone resorption on its opposing<br />
surface.<br />
Ethmomaxillary complex: the upper part of<br />
the face, mostly comprising the ethmoid, the<br />
nasal capsule, <strong>and</strong> the maxilla.<br />
Facial projection: degree to which face<br />
projects in front of <strong>cranial</strong> <strong>base</strong>; measured<br />
here by nasion-foramen caecum.<br />
Integration: the genetic, epigenetic, or <strong>function</strong>al<br />
association among elements via “a set<br />
causal mechanisms so that change in one<br />
element is reflected by change in another”<br />
(Smith, 1996). <strong>The</strong> results of integration are<br />
most often recognized as a pattern of significant,<br />
hierarchical covariation among the<br />
components of a system.<br />
Kyphosis: angle of some aspect of facial orientation<br />
relative to the neuro- <strong>and</strong>/or basicranium,<br />
measured here using angle of facial<br />
kyphosis (AFK) for the orientation of<br />
the palate, <strong>and</strong> angle of orbit axis orientation<br />
(AOA) for orientation of the orbital axis.<br />
Planum sphenoideum: midline “plane” of<br />
the anterior <strong>cranial</strong> <strong>base</strong> from the sphenoidale<br />
(Sp) to the planum sphenoideum (PS)<br />
point (see below).
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 119<br />
Postchordal <strong>cranial</strong> <strong>base</strong>: portion of the <strong>cranial</strong><br />
<strong>base</strong> posterior to the sella; frequently<br />
called the posterior <strong>cranial</strong> <strong>base</strong>.<br />
Prechordal <strong>cranial</strong> <strong>base</strong>: portion of the <strong>cranial</strong><br />
<strong>base</strong> anterior to sella; frequently called<br />
the anterior <strong>cranial</strong> <strong>base</strong>.<br />
Telencephalon: forebrain, consisting of<br />
paired olfactory lobes, the basal ganglia,<br />
<strong>and</strong> the neocortex.<br />
LANDMARK DEFINITIONS<br />
Ba, basion: midsagittal point on anterior<br />
margin of foramen magnum.<br />
CP, clival point: midline point on basioccipital<br />
clivus inferior to point at which dorsum<br />
sellae curves posteriorly.<br />
FC, foramen caecum: pit on cribriform plate<br />
between crista galli <strong>and</strong> endo<strong>cranial</strong> wall of<br />
frontal bone.<br />
H, hormion: most posterior midline point on<br />
vomer.<br />
OA: supero-inferior midpoint between superior<br />
orbital fissures <strong>and</strong> inferior rims of optic<br />
canals; for mammals without completely<br />
enclosed orbits, OA is defined as inferior rim<br />
of optic foramen.<br />
OM: supero-inferior midpoint between<br />
lower <strong>and</strong> upper orbital rims.<br />
Op, opisthion: most posterior point in foramen<br />
magnum.<br />
PMp, PM point: average of projected midline<br />
points of most anterior point on lamina<br />
of greater wings of sphenoid.<br />
PP, pituitary point: “the anterior edge of<br />
the groove for the optic chiasma, just in<br />
front of the pituitary fossa” (Zuckerman,<br />
1955).<br />
PS, planum sphenoideum point: most superior<br />
midline point on sloping surface in<br />
which cribriform plate is set.<br />
Ptm, pterygomaxillare: average of projected<br />
midline points of most inferior <strong>and</strong> posterior<br />
points on maxillary tuberosities.<br />
S, sella: center of sella turcica, independent<br />
of contours of clinoid processes.<br />
Sb, sphenobasion: midline point on sphenooccipital<br />
synchondrosis on external aspect of<br />
clivus.<br />
Sp, sphenoidale: most posterior, superior<br />
midline point of planum sphenoideum.<br />
ANGLE, LINE, AND PLANE DEFINITIONS<br />
AOA: orbital axis orientation relative to CO<br />
(Ross <strong>and</strong> Ravosa, 1993).<br />
BL1: Ba-PP PP-Sp (Ross <strong>and</strong> Ravosa,<br />
1993; Ross <strong>and</strong> Henneberg, 1995).<br />
BL2: Ba-S S-FC (Spoor, 1997).<br />
CBA1: Ba-S relative to S-FC (Lieberman<br />
<strong>and</strong> McCarthy, 1999).<br />
CBA2: Ba-S relative to Sp-PS (Lieberman<br />
<strong>and</strong> McCarthy, 1999).<br />
CBA3: Ba-CP relative to S-FC (Lieberman<br />
<strong>and</strong> McCarthy, 1999).<br />
CBA4: Ba-CP relative to Sp-PS (Lieberman<br />
<strong>and</strong> McCarthy, 1999).<br />
CO, clivus ossis occipitalis: endo<strong>cranial</strong> line<br />
from Ba to spheno-occipital synchondrosis<br />
(Ross <strong>and</strong> Ravosa, 1993).<br />
External CBA (CBA5): angle between basionsphenobasion-hormion<br />
(Lieberman <strong>and</strong> Mc-<br />
Carthy, 1999).<br />
FM, foramen magnum: Ba-Op.<br />
Forel’s axis: from most antero-inferior point<br />
on frontal lobe to most postero-inferior point<br />
on occipital lobe (Hofer, 1969).<br />
Head-neck angle: orientation of head relative<br />
to neck in locomoting animals, calculated<br />
as neck inclination orbit inclination<br />
(Strait <strong>and</strong> Ross, 1999).<br />
IRE1: cube root of endo<strong>cranial</strong> volume/BL 1<br />
(Ross <strong>and</strong> Ravosa, 1993).<br />
IRE2: cube root of neocortical volume/BL 1<br />
(Ross <strong>and</strong> Ravosa, 1993).<br />
IRE3: cube root of telencephalon volume/BL<br />
1 (Ross <strong>and</strong> Ravosa, 1993).<br />
IRE4: cube root of neocortical volume/palate<br />
length (Ross <strong>and</strong> Ravosa, 1993).<br />
IRE5: cube root of endo<strong>cranial</strong> volume/BL 2<br />
(McCarthy, 2001).<br />
Meynert’s axis: from ventral edge of junction<br />
between pons <strong>and</strong> medulla to caudal<br />
recess of interpeduncular fossa (Hofer,<br />
1969).<br />
Neck inclination: orientation of surface of<br />
neck relative to substrate (Strait <strong>and</strong> Ross,<br />
1999).<br />
NHA: neutral horizontal axis of orbits; from<br />
OM to OA (Enlow <strong>and</strong> Azuma, 1975).<br />
Orbital axis orientation: line from optic foramen<br />
through superoinferior midpoint of<br />
orbital aperture (Ravosa, 1988).<br />
Orbit inclination: orientation relative to<br />
substrate of a line joining superior <strong>and</strong> in-
120 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
ferior margins of orbits (Strait <strong>and</strong> Ross,<br />
1999).<br />
PM plane, posterior maxillary plane: from<br />
Ptm to PMp (Enlow <strong>and</strong> Azuma, 1975).<br />
INTRODUCTION<br />
<strong>The</strong> <strong>cranial</strong> <strong>base</strong> has important integrative<br />
<strong>and</strong> <strong>function</strong>al roles in the skull, many<br />
of which reflect its phylogenetic history as<br />
the oldest component of the vertebrate skull<br />
(de Beer, 1937). Architecturally, the <strong>cranial</strong><br />
<strong>base</strong> provides the platform upon which the<br />
brain grows <strong>and</strong> around which the face<br />
grows. In addition, the <strong>cranial</strong> <strong>base</strong> connects<br />
the cranium with the rest of the body:<br />
it articulates with the vertebral column <strong>and</strong><br />
the m<strong>and</strong>ible, provides conduits for all the<br />
vital neural <strong>and</strong> circulatory connections between<br />
the brain <strong>and</strong> the face <strong>and</strong> neck,<br />
houses <strong>and</strong> connects the sense organs in the<br />
skull, <strong>and</strong> forms the roof of the nasopharynx.<br />
<strong>The</strong> shape of the <strong>cranial</strong> <strong>base</strong> is therefore<br />
a multifactorial product of numerous<br />
phylogenetic, developmental, <strong>and</strong> <strong>function</strong>al<br />
interactions.<br />
<strong>The</strong> importance of the <strong>cranial</strong> <strong>base</strong> is<br />
matched by several challenges that make it<br />
difficult to study. Because the <strong>cranial</strong> <strong>base</strong><br />
is difficult to access surgically, there have<br />
been few experimental studies of <strong>cranial</strong><br />
<strong>base</strong> growth <strong>and</strong> <strong>function</strong>. Also, a large proportion<br />
of the <strong>cranial</strong> <strong>base</strong> is not only complex<br />
anatomically, but is also difficult to<br />
measure <strong>and</strong>/or see externally. In addition,<br />
the <strong>cranial</strong> <strong>base</strong> in many fossils is missing,<br />
damaged, or unobservable without special<br />
technology. However, new developmental<br />
studies, <strong>and</strong> new techniques for imaging,<br />
have led to a modest renaissance of research<br />
on <strong>cranial</strong> <strong>base</strong> morphology (reviewed in<br />
Spoor et al., 2000). In addition, new analytical<br />
techniques which quantitatively compare<br />
three-dimensional differences in form<br />
have opened up new possibilities for studying<br />
growth <strong>and</strong> variation in complex regions<br />
such as the <strong>cranial</strong> <strong>base</strong> (Cheverud <strong>and</strong><br />
Richtsmeier, 1986; Bookstein, 1991; Lele,<br />
1993; O’Higgins, 2000). Ultimately, better<br />
information about the relationships between<br />
<strong>cranial</strong> <strong>base</strong> morphology <strong>and</strong> the rest<br />
of the skull may help to resolve a number of<br />
important phylogenetic <strong>and</strong> behavioral issues<br />
throughout <strong>primate</strong> evolution.<br />
<strong>The</strong> goals of this review are to provide a<br />
background on key aspects of <strong>cranial</strong> <strong>base</strong><br />
growth <strong>and</strong> development necessary to formulate<br />
or test hypotheses about the role of<br />
the <strong>cranial</strong> <strong>base</strong> in <strong>cranial</strong> growth, integration,<br />
<strong>and</strong> <strong>function</strong>. <strong>The</strong>refore, we review recent<br />
research on <strong>cranial</strong> <strong>base</strong> variation, development,<br />
<strong>and</strong> evolution in <strong>primate</strong>s,<br />
focusing on the major dimensions of the <strong>cranial</strong><br />
<strong>base</strong> (especially width, length, <strong>and</strong> angulation<br />
in the sagittal plane). Other, more<br />
detailed aspects of <strong>cranial</strong> <strong>base</strong> anatomy<br />
<strong>and</strong> morphology, most notably the inner ear,<br />
were recently reviewed by Spoor <strong>and</strong> Zonneveld<br />
(1998) <strong>and</strong> will not be covered in this<br />
review (see also Braga et al., 1999). Where<br />
relevant, we have made an effort to include<br />
data from the few experimental studies on<br />
<strong>cranial</strong> <strong>base</strong> growth <strong>and</strong> <strong>function</strong>. Most experimental<br />
research on the mammalian<br />
skull has focused on the face <strong>and</strong> neurocranium;<br />
however, some of these studies provide<br />
indirect clues on interrelationships<br />
among the brain, <strong>cranial</strong> <strong>base</strong>, <strong>and</strong> face<br />
(e.g., Sarnat, 1988, 1999). Finally, we conclude<br />
with a short discussion of two main<br />
issues which we believe require further research<br />
to address: what factors determine<br />
most of the variation in <strong>cranial</strong> <strong>base</strong> shape<br />
among <strong>primate</strong>s, <strong>and</strong> to what extent does<br />
variation in <strong>cranial</strong> <strong>base</strong> form influence ontogenetic<br />
<strong>and</strong> interspecific patterns of variation<br />
in craniofacial morphology?<br />
ANATOMY AND DEVELOPMENT<br />
A detailed underst<strong>and</strong>ing of the series of<br />
events <strong>and</strong> underlying mechanisms that<br />
generate patterns 1 of morphological variation<br />
in the basicranium is vital for developing<br />
<strong>and</strong> testing hypotheses about the <strong>cranial</strong><br />
<strong>base</strong>’s role in craniofacial integration<br />
Please address all correspondence to: Daniel E. Lieberman,<br />
Department of Anthropology, George Washington <strong>University</strong>,<br />
2110 G St, Washington DC 20052.<br />
E-mail: danliebgwu.edu; phone: 202-994-0873; fax: 202-994-<br />
6097.<br />
1 <strong>The</strong> term “pattern” here refers to a static description of a<br />
configuration or relationship among things, whereas “process”<br />
refers to a series of events that occur during something’s formation.<br />
Note that we do not define process here as a causal mechanism.<br />
Most of the processes described here have multiple <strong>and</strong><br />
hierarchical levels of causation which merit further study.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 121<br />
Fig. 1. Chondrocranium in Homo sapiens (after<br />
Sperber, 1989). A: Superior view of chondro<strong>cranial</strong> precursors<br />
<strong>and</strong> ossification centers (after Sperber, 1989).<br />
Primordial cartilages are at right, <strong>and</strong> their <strong>cranial</strong><br />
<strong>base</strong> derivatives are on left. Note that the nasal capsule<br />
forms the ethmoid, the inferior concha, <strong>and</strong> the nasal<br />
septum; the presphenoid forms the sphenoid body; the<br />
orbitosphenoid forms the lesser wing of the sphenoid;<br />
the alisphenoid forms the greater wing of the sphenoid;<br />
the postsphenoid forms the sella turcica; the otic capsule<br />
forms the petrous temporal; the parachordal forms<br />
the basioccipital; <strong>and</strong> the occipital sclerotomes form the<br />
exoccipital. B: Lateral view of chondro<strong>cranial</strong> precursors<br />
in a fetus 8 weeks i.u.<br />
<strong>and</strong> <strong>function</strong>. So we begin with a brief summary<br />
of <strong>cranial</strong> <strong>base</strong> embryology, fetal<br />
growth, <strong>and</strong> postnatal growth. Most of the<br />
information summarized below derives from<br />
studies of human basi<strong>cranial</strong> growth <strong>and</strong><br />
development; the majority of these patterns<br />
<strong>and</strong> processes are generally applicable to all<br />
<strong>primate</strong>s, but we tried to distinguish those<br />
that are unique to humans or other species.<br />
Further information is available in Björk<br />
(1955), Ford (1958), Scott (1958), Moore <strong>and</strong><br />
Lavelle (1974), Starck (1975), Bosma (1976),<br />
Moss et al. (1982), Slavkin (1989), Sperber<br />
(1989), Enlow (1990), <strong>and</strong> Jeffery (1999), as<br />
well as the many references cited below.<br />
Development of the chondrocranium<br />
<strong>The</strong> human <strong>cranial</strong> <strong>base</strong> first appears in<br />
the second month of embryonic life as a<br />
narrow, irregularly shaped cartilaginous<br />
platform, the chondrocranium, ventral to<br />
the embryonic brain. <strong>The</strong> chondrocranium<br />
develops between the <strong>base</strong> of the embryonic<br />
brain <strong>and</strong> foregut about 28 days intra utero<br />
(i.u.) as condensations of neural crest cells<br />
(highly mobile, pluripotent neurectodermal<br />
cells that make up most of the head) <strong>and</strong><br />
paraxial mesoderm in the ectomeninx (a<br />
mesenchyme-derived membrane surrounding<br />
the brain) (Sperber, 1989). By the seventh<br />
week i.u., the ectomeninx has grown<br />
around the <strong>base</strong> of the brain <strong>and</strong> differentiated<br />
into nine groups of paired cartilagenous<br />
precursors (Fig. 1A,B) (Kjaer, 1990).<br />
From caudal to rostral these are: 1) four<br />
occipital condensations on either side of the<br />
future brain stem derived from sclerotomic<br />
portions of postotic somites; 2) a pair of<br />
parachordal cartilages on either side of the<br />
primitive notochord; 3) the otic capsules, lying<br />
lateral to the parachordal cartilages; 4)<br />
the hypophyseal (polar) cartilages which<br />
surround the anterior pituitary gl<strong>and</strong>; 5–6)<br />
the orbitosphenoids (ala orbitalis/lesser<br />
wing of sphenoid) <strong>and</strong> alisphenoids (ala<br />
temporalis/greater wings of sphenoid)<br />
which lie lateral to the hypophyseal cartilages;<br />
7–8) the trabecular cartilages which<br />
form the mesethmoid <strong>and</strong>, more laterally,<br />
the nasal capsule cartilages; <strong>and</strong> 9) the ala<br />
hypochiasmatica which, together with parts<br />
of the trabecular <strong>and</strong> orbitosphenoid cartilages,<br />
forms the presphenoid.<br />
<strong>The</strong> chondro<strong>cranial</strong> precursors anterior to<br />
the notochord (groups 5–9) derive solely<br />
from segmented neural crest tissue (somitomeres),<br />
while the posterior precursors<br />
(groups 1–4) derive from segmented mesodermal<br />
tissue (somites) (Noden, 1991; Couly<br />
et al., 1993; Le Douarin et al., 1993). Consequently,<br />
the middle of the sphenoid body<br />
(the mid-sphenoidal synchondrosis) marks<br />
the division between the anterior (prechordal)<br />
<strong>and</strong> posterior (postchordal) portions of<br />
the <strong>cranial</strong> <strong>base</strong> that are embryologically<br />
distinct. Antero-posterior specification of<br />
the segmental precursors of the <strong>cranial</strong> <strong>base</strong><br />
is complex <strong>and</strong> still incompletely known, but
122 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
appears to mostly involve the expression of<br />
the Hox <strong>and</strong> Dlx gene clusters (Lufkin et al.,<br />
1992; Robinson <strong>and</strong> Mahon, 1994; Vielle-<br />
Grosjean et al., 1997). For recent summaries<br />
of pattern formation <strong>and</strong> gene expression<br />
in the vertebrate <strong>cranial</strong> <strong>base</strong>, see<br />
Langille <strong>and</strong> Hall (1993) <strong>and</strong> Schilling <strong>and</strong><br />
Thorogood (2000).<br />
At least 41 ossification centers, which begin<br />
to appear in the chondrocranium about<br />
8 weeks i.u., are responsible for the transformation<br />
of the chondrocranium into the<br />
basicranium (Sperber, 1989; Kjaer, 1990).<br />
<strong>The</strong>se centers (Fig. 1B) form within a perforated<br />
<strong>and</strong> highly irregularly shaped platform<br />
known as the basal plate. In general,<br />
ossification begins with the mesodermally<br />
derived cartilages toward the caudal end of<br />
the chondrocranium, <strong>and</strong> proceeds rostrally<br />
<strong>and</strong> laterally, eventually forming the four<br />
major bones that comprise the <strong>primate</strong> basicranium:<br />
the ethmoid, most of the sphenoid,<br />
<strong>and</strong> parts of the occipital <strong>and</strong> temporal<br />
bones (which also include some intramembranous<br />
elements). <strong>The</strong> sequence in which<br />
the four bones of the <strong>cranial</strong> <strong>base</strong> ossify from<br />
the chondrocranium is complex, <strong>and</strong> still<br />
not entirely resolved (reviewed in Sperber,<br />
1989; Williams et al., 1995; Jeffery, 1999),<br />
but we highlight here the major steps, proceeding<br />
from caudal to rostral. <strong>The</strong> occipital<br />
comprises four bones surrounding the foramen<br />
magnum. <strong>The</strong> squamous portion is primarily<br />
intramembranous bone of the <strong>cranial</strong><br />
vault, except for the nuchal region,<br />
which ossifies endochondrally from two separate<br />
centers (Srivastava, 1992) <strong>and</strong> fuses<br />
with the lateral exoccipitals on either side of<br />
the foramen magnum that fuse with the<br />
basioccipital. <strong>The</strong> sphenoid body forms from<br />
fusion of the presphenoids <strong>and</strong> basisphenoid<br />
around the pituitary, forming the sella turcica<br />
(“Turkish saddle”). <strong>The</strong> greater <strong>and</strong><br />
lesser wings of the sphenoid develop from<br />
the fusion of the alisphenoid <strong>and</strong> orbitosphenoid<br />
cartilages to the body (Kodama,<br />
1976a–c; Sasaki <strong>and</strong> Kodama, 1976). Later,<br />
the medial <strong>and</strong> lateral pterygoid plates <strong>and</strong><br />
portions of the greater wings ossify intramembraneously.<br />
<strong>The</strong> temporals, which<br />
form much of the lateral aspect of the basicranium,<br />
develop from approximately 21 ossification<br />
centers, several of which are intramembranous,<br />
including the squamous,<br />
tympanic, <strong>and</strong> zygomatic regions (Shapiro<br />
<strong>and</strong> Robinson, 1980; Sperber, 1989). <strong>The</strong> petrous<br />
<strong>and</strong> mastoid parts of the temporal<br />
form the inner ear from the otic capsule, <strong>and</strong><br />
the styloid process of the temporal ossifies<br />
from cartilage in the second branchial arch.<br />
<strong>The</strong> ethmoid, which is entirely endochondral<br />
in origin, forms the center of the anterior<br />
<strong>cranial</strong> floor, <strong>and</strong> most of the nasal cavity<br />
from three ossification centers in the<br />
mesethmoid <strong>and</strong> nasal capsule cartilages<br />
(Hoyte, 1991). An additional cartilaginous<br />
ossification center detaches from the ectethmoid<br />
to form a separate scrolled bone, the<br />
inferior nasal concha, inside the nasal cavity.<br />
Patterns <strong>and</strong> processes of basi<strong>cranial</strong><br />
growth<br />
In order to underst<strong>and</strong> how the basicranium<br />
grows <strong>and</strong> <strong>function</strong>s during the fetal<br />
<strong>and</strong> postnatal periods, it is useful to keep in<br />
mind three important principles of basi<strong>cranial</strong><br />
development. First, the center of the<br />
basicranium (an oval-shaped region around<br />
the sphenoid body) attains adult size <strong>and</strong><br />
shape more rapidly than the anterior, posterior,<br />
<strong>and</strong> lateral portions, presumably because<br />
almost all the vital <strong>cranial</strong> nerves <strong>and</strong><br />
major vessels perforate the <strong>cranial</strong> <strong>base</strong> in<br />
this region (Figs. 1A, 2) (Sperber, 1989).<br />
Second, the prechordal (anterior) <strong>and</strong> postchordal<br />
(posterior) <strong>cranial</strong> <strong>base</strong> grow somewhat<br />
independently, perhaps reflecting<br />
their distinct embryonic origins <strong>and</strong> their<br />
different spatial <strong>and</strong> <strong>function</strong>al roles (outlined<br />
above). Third, most basi<strong>cranial</strong> growth<br />
in the three <strong>cranial</strong> fossae occurs independently<br />
(Fig. 2). <strong>The</strong> posterior <strong>cranial</strong> fossa,<br />
which houses the occipital lobes <strong>and</strong> the<br />
brain stem (the cerebellum <strong>and</strong> the medulla<br />
oblongata), is bounded laterally by the petrous<br />
<strong>and</strong> mastoid portions of the temporal<br />
bone, <strong>and</strong> anteriorly by the dorsum sellae of<br />
the sphenoid. <strong>The</strong> butterfly-shaped middle<br />
<strong>cranial</strong> fossa, which supports the temporal<br />
lobes <strong>and</strong> the pituitary gl<strong>and</strong>, is bounded<br />
posteriorly by the dorsum sellae <strong>and</strong> the<br />
petrous portions of the temporal, <strong>and</strong> anteriorly<br />
by the posterior borders of the lesser<br />
wings of the sphenoid, <strong>and</strong> by the anterior<br />
clinoid processes of the sphenoid. <strong>The</strong> ante-
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 123<br />
Fig. 2. Superior view of human <strong>cranial</strong> <strong>base</strong> (after<br />
Enlow, 1990). Left: Division between anterior <strong>cranial</strong><br />
fossa (ACF), middle <strong>cranial</strong> fossa (MCF), <strong>and</strong> posterior<br />
<strong>cranial</strong> fossa (PCF). Right: Locations of major foramina<br />
(in black), <strong>and</strong> distribution of resorptive growth fields<br />
(dark, with ) <strong>and</strong> depository growth fields (light, with ).<br />
rior <strong>cranial</strong> fossa, which houses the frontal<br />
lobe <strong>and</strong> the olfactory bulbs, is bounded posteriorly<br />
by the lesser wings of the sphenoid.<br />
Following its initial formation, the <strong>cranial</strong><br />
<strong>base</strong> grows in a complex series of events,<br />
largely through displacement <strong>and</strong> drift (see<br />
Glossary). Four main types of growth occur<br />
within <strong>and</strong> between the endo<strong>cranial</strong> fossae:<br />
antero-posterior growth through displacement<br />
<strong>and</strong> drift; medio-lateral growth<br />
through displacement <strong>and</strong> drift; supero-inferior<br />
growth through drift; <strong>and</strong> angulation<br />
(primarily flexion <strong>and</strong> extension). In order<br />
to review how these types of growth occur,<br />
we will focus primarily on the sequence of<br />
events <strong>and</strong> patterns of basi<strong>cranial</strong> growth in<br />
humans <strong>and</strong> their major differences from<br />
nonhuman <strong>primate</strong>s.<br />
Antero-posterior growth. Basi<strong>cranial</strong><br />
elongation during <strong>ontogeny</strong> occurs in three<br />
ways: 1) drift at the anterior <strong>and</strong> posterior<br />
margins of the <strong>cranial</strong> <strong>base</strong>; 2) displacement<br />
in coronally oriented sutures such as the<br />
fronto-sphenoid; <strong>and</strong> 3) displacement in the<br />
midline of the <strong>cranial</strong> <strong>base</strong> from growth<br />
within the three synchondroses: the midsphenoid<br />
synchondrosis (MSS), the sphenoethmoid<br />
synchondrosis (SES), <strong>and</strong> the spheno-occipital<br />
synchondrosis (SOS). During<br />
the fetal period in both humans <strong>and</strong> nonhuman<br />
<strong>primate</strong>s, the midline anterior <strong>cranial</strong><br />
<strong>base</strong> grows in a pattern of positive allometry<br />
(mostly through ethmoidal growth) relative<br />
to the midline posterior <strong>cranial</strong> <strong>base</strong> (Ford,<br />
1956; Sirianni <strong>and</strong> Newell-Morris, 1980;<br />
Sirianni, 1985; Anagnostopolou et al., 1988;<br />
Sperber, 1989; Hoyte, 1991; Jeffrey, 1999).<br />
During fetal growth, several key differences<br />
emerge between humans <strong>and</strong> other <strong>primate</strong>s<br />
in the relative proportioning of the<br />
posterior <strong>cranial</strong> fossa (Fig. 3). In humans,<br />
antero-posterior growth in the basioccipital<br />
is proportionately less than in the exoccipital<br />
<strong>and</strong> squamous occipital posterior to the<br />
foramen magnum, whereas the pattern is<br />
apparently reversed in nonhuman <strong>primate</strong>s,<br />
with proportionately more growth in<br />
the basioccipital (Ford, 1956; Moore <strong>and</strong><br />
Lavelle, 1974). <strong>The</strong> nuchal plane rotates<br />
downward to become more horizontal in humans,<br />
but rotates in the reverse direction to<br />
become more vertical in nonhuman <strong>primate</strong>s,<br />
apparently because of a growth field<br />
reversal (Fig. 3). According to Duterloo <strong>and</strong><br />
Enlow (1970), the inside <strong>and</strong> outside of the<br />
nuchal plane in humans are resorptive <strong>and</strong><br />
depository growth fields, respectively; but in<br />
nonhuman <strong>primate</strong>s, the inside <strong>and</strong> outside<br />
of the nuchal plane are reported to be depository<br />
<strong>and</strong> resorptive growth fields, respectively.<br />
As a result, the foramen magnum<br />
lies close to the center of the<br />
basicranium in the human neonate <strong>and</strong><br />
more posteriorly in nonhuman <strong>primate</strong>s<br />
(Zuckerman, 1954, 1955; Schultz, 1955;<br />
Ford, 1956; Biegert, 1963; Crelin, 1969).<br />
Postnatally, the posterior <strong>cranial</strong> <strong>base</strong><br />
primarily elongates in the midline through<br />
deposition in the SOS <strong>and</strong> through posterior<br />
drift of the foramen magnum; more laterally,<br />
the posterior <strong>cranial</strong> fossa elongates<br />
through deposition in the occipitomastoid<br />
suture <strong>and</strong> through posterior drift. In all<br />
<strong>primate</strong>s, the basioccipital lengthens approximately<br />
twofold after birth, with rapid
124 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Fig. 3. Midsagittal view of nonhuman <strong>primate</strong> (A) human (B), showing different patterns of drift of<br />
occipital, <strong>and</strong> position of foramen magnum, relative to overall <strong>cranial</strong> length in the Frankfurt horizontal.<br />
FM, center of the foramen magnum; OP (opisthocranium) <strong>and</strong> PR (prosthion) are, respectively the most<br />
posterior <strong>and</strong> anterior points on the skull in the Frankfurt horizontal. , depository surfaces; <br />
resorptive surfaces.<br />
growth during the neural growth period<br />
(e.g., up to approximately 6 years in humans)<br />
<strong>and</strong> some additional elongation occurring<br />
through the adolescent growth<br />
spurt (Ashton <strong>and</strong> Spence, 1958; Scott,<br />
1958; Riolo et al., 1974; Sirianni <strong>and</strong> Swindler,<br />
1979; Sirianni, 1985). <strong>The</strong> SOS contributes<br />
to roughly 70% of posterior <strong>cranial</strong><br />
<strong>base</strong> elongation in macaques (Sirianni <strong>and</strong><br />
Van Ness, 1978). <strong>The</strong> rest of posterior basi<strong>cranial</strong><br />
growth in nonhuman <strong>primate</strong>s occurs<br />
through posterior drift of the foramen<br />
magnum, which has been shown by fluorochrome<br />
dye labeling experiments to migrate<br />
caudally in nonhuman <strong>primate</strong>s through resorption<br />
at its posterior end <strong>and</strong> deposition<br />
at its anterior end (Michejda, 1971; Giles et<br />
al., 1981). In contrast, the foramen magnum<br />
remains in the center of the human skull<br />
<strong>base</strong>, roughly halfway between the most anterior<br />
<strong>and</strong> posterior points of the skull<br />
(Lugoba <strong>and</strong> Wood, 1990). <strong>The</strong> posterior <strong>cranial</strong><br />
<strong>base</strong> in H. sapiens still elongates during<br />
postnatal growth, but to a lesser degree<br />
than in nonhuman <strong>primate</strong>s.<br />
Postnatal elongation in the anterior <strong>cranial</strong><br />
<strong>base</strong> is somewhat more complex because<br />
of its multiple roles in neural <strong>and</strong><br />
facial growth. <strong>The</strong> anterior <strong>cranial</strong> <strong>base</strong><br />
(measured from sella to foramen caecum)<br />
elongates in concert with the frontal lobes of<br />
the brain, reaching approximately 95% of<br />
its adult length by the end of the neural<br />
growth period (e.g., 6 years in humans, 3<br />
years in chimpanzees, <strong>and</strong> 1.2 years in macaques)<br />
(Scott, 1958; Sirianni <strong>and</strong> Newell-<br />
Morris, 1978; Sirianni <strong>and</strong> Van Ness, 1978;<br />
Lieberman, 1998). Postnatal anterior <strong>cranial</strong><br />
<strong>base</strong> elongation can occur in the SES (in<br />
the midline), through displacement in the<br />
sphenoid-frontal suture, <strong>and</strong> through drift<br />
of the anterior margin of the frontal bone. In<br />
humans, however, the SES remains active<br />
<strong>and</strong> unfused until 6–8 years after birth,<br />
when the brain has completed most of its<br />
growth, but the SES apparently fuses near<br />
birth in nonhuman <strong>primate</strong>s (Michejda <strong>and</strong><br />
Lamey, 1971). <strong>The</strong>se differences in the timing<br />
<strong>and</strong> sequence of synchondroseal activity<br />
<strong>and</strong> fusion may be related to the different<br />
relative contributions of the lesser wings of<br />
the sphenoid <strong>and</strong> the frontal to the anterior<br />
<strong>cranial</strong> floor in humans <strong>and</strong> nonhuman <strong>primate</strong>s.<br />
Although there is some intraspecific<br />
variation, the lesser wing of the sphenoid in<br />
humans tends to comprise approximately<br />
one third of the <strong>cranial</strong> floor, extending all<br />
the way to the cribriform plate; in nonhuman<br />
<strong>primate</strong>s, the cribriform usually lies<br />
entirely within the ethmoid (Fig. 4), <strong>and</strong> the
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 125<br />
Fig. 4. Superior view of <strong>cranial</strong> <strong>base</strong> in Homo sapiens (left) <strong>and</strong> Pan troglodytes (right) (after Aiello<br />
<strong>and</strong> Dean, 1991). FC, foramen, caecum; PS, planum sphenoideum point; SP, sphenoidale; S, sella. Note<br />
similar orientation of the inferior petrosal posterior surface (PPip) in the two species (data from Spoor,<br />
1997). In addition, the lesser wing of the sphenoid <strong>and</strong> the cribriform plate comprise a much greater<br />
percentage of the midline anterior <strong>cranial</strong> <strong>base</strong> in humans than in chimpanzees.<br />
lesser wing of the sphenoid makes up less<br />
than one tenth of the <strong>cranial</strong> floor (Van der<br />
Linden <strong>and</strong> Enlow, 1971; Aiello <strong>and</strong> Dean,<br />
1990; McCarthy, 2001). Differences in the<br />
sequence of synchondroseal fusion may also<br />
be related to differences in the timing <strong>and</strong><br />
nature of <strong>cranial</strong> <strong>base</strong> angulation in human<br />
vs. nonhuman <strong>primate</strong>s (Jeffery, 1999; see<br />
below).<br />
While the anterior <strong>cranial</strong> <strong>base</strong> grows<br />
solely during the neural growth phase (it<br />
reaches adult size at the same time as the<br />
brain), the more inferior portions of the<br />
anterior <strong>cranial</strong> <strong>base</strong> continue to grow as<br />
part of the face after the neural growth<br />
phase, forming the ethmomaxillary complex<br />
(Enlow, 1990). This complex grows<br />
downward <strong>and</strong> forward mostly through<br />
drift <strong>and</strong> displacement. In addition, the<br />
sphenoid sinus drifts anteriorly. Since the<br />
ethmoid (with the exception of the cribriform<br />
plate) primarily grows as part of the<br />
ethmomaxillary complex, its postnatal<br />
growth is most properly treated in a review<br />
of facial growth.<br />
Medio-lateral growth. How the <strong>cranial</strong><br />
<strong>base</strong> widens is important because of its various<br />
interactions with neuro<strong>cranial</strong> <strong>and</strong> facial<br />
shape (Lieberman et al., 2000; see below).<br />
<strong>The</strong> increases in width of the anterior<br />
<strong>and</strong> posterior <strong>cranial</strong> fossae occur primarily<br />
from drift (in which the external <strong>and</strong> internal<br />
surfaces of the squamae are depository<br />
<strong>and</strong> resorptive, respectively), <strong>and</strong> from intramembranous<br />
bone growth in sutures<br />
with some component of lateral orientation,<br />
such as the fronto-ethmoid <strong>and</strong> occipitomastoid<br />
sutures (Sperber, 1989). Lateral<br />
growth in the middle <strong>cranial</strong> fossa is slightly<br />
more complicated. <strong>The</strong> sphenoid body does<br />
not widen much (Kodama, 1976a,b; Sasaki<br />
<strong>and</strong> Kodama, 1976). Instead, most increases<br />
in middle <strong>cranial</strong> fossa width presumably<br />
occur in the spheno-temporal suture <strong>and</strong><br />
through lateral drift of the squamous portions<br />
of the sphenoid.<br />
Increases in cerebellum <strong>and</strong> brain-stem<br />
size have been implicated in changes in the<br />
orientation of the petrous pyramids (Fig. 4),<br />
which are more coronally oriented externally<br />
(but not internally) in humans than in<br />
nonhuman <strong>primate</strong>s (Dean, 1988). Spoor<br />
(1997) found that petrous pyramid orientation<br />
in a broad interspecific sample of pri-
126 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
mates was significantly negatively correlated<br />
with relative brain size (r 0.85,<br />
P 0.001) but not with the <strong>cranial</strong> <strong>base</strong><br />
angle. However, Jeffery (1999) found that<br />
petrous pyramid orientation is independent<br />
of relative brain size in fetal humans (during<br />
the second trimester).<br />
Supero-inferior growth. Most brain<br />
growth apparently causes the neurocranium<br />
<strong>and</strong> parts of the basicranium to grow<br />
superiorly, anteriorly, <strong>and</strong> laterally (de<br />
Beer, 1937). However, the endo<strong>cranial</strong> fossae<br />
also become slightly deeper through<br />
drift because most of the endo<strong>cranial</strong> floor is<br />
resorptive, while the inferior side of the basicranium<br />
is depository (Fig. 2) (Duterloo<br />
<strong>and</strong> Enlow, 1970; Enlow, 1990). <strong>The</strong> endo<strong>cranial</strong><br />
margins between the fossae that<br />
separate the different portions of the brain<br />
(the petrous portion of the temporal <strong>and</strong> the<br />
lesser wing of the sphenoid) do not drift<br />
inferiorly because they remain depository<br />
surfaces (Enlow, 1976). Differences in drift<br />
most likely reflect variation in the relative<br />
size of the components of the brain in conjunction<br />
with other spatial relationships<br />
among components of the skull. In particular,<br />
inferior drift of the anterior <strong>cranial</strong><br />
fossa is presumably minimal because it<br />
would impinge upon the orbits <strong>and</strong> nasal<br />
cavity that lie immediately below. <strong>The</strong> only<br />
exception is the cribriform plate which<br />
drifts inferiorly, slightly in humans (Moss,<br />
1963), but sometimes forming a “deep olfactory<br />
pit” in many species of nonhuman <strong>primate</strong>s<br />
(Cameron, 1930; Aiello <strong>and</strong> Dean,<br />
1990). Inferior drift of the middle <strong>cranial</strong><br />
fossa presumably reflects inferiorly directed<br />
growth of the temporal lobes, but this hypothesis<br />
has not been tested. Likewise, inferior<br />
drift in the posterior <strong>cranial</strong> fossa,<br />
which is shallow in most nonhuman <strong>primate</strong>s,<br />
is hypothesized to be a <strong>function</strong> of<br />
the size of the occipital lobes, the cerebellum,<br />
<strong>and</strong> the brain stem below the tentorium<br />
cerebelli. Note that <strong>cranial</strong> <strong>base</strong> flexion<br />
during growth, which occurs uniquely in<br />
humans (see below), complements inferior<br />
drift in the posterior <strong>cranial</strong> fossa by moving<br />
the floor of the posterior <strong>cranial</strong> fossa more<br />
below the middle <strong>cranial</strong> fossa.<br />
Angulation. Angulation of the <strong>cranial</strong><br />
<strong>base</strong> occurs when the prechordal <strong>and</strong> postchordal<br />
portions of the basicranium flex or<br />
extend relative to each other in the midsagittal<br />
plane (technically, flexion <strong>and</strong> extension<br />
describe a series of events in which the<br />
angle between the inferior or ventral surfaces<br />
of the <strong>cranial</strong> <strong>base</strong> decrease or increase,<br />
respectively). Angulation has been<br />
the subject of much research because flexion<br />
<strong>and</strong> extension of the <strong>cranial</strong> <strong>base</strong> affect the<br />
relative positions of the three endo<strong>cranial</strong><br />
fossae, thereby influencing a wide range of<br />
spatial relationships among the <strong>cranial</strong><br />
<strong>base</strong>, brain, face, <strong>and</strong> pharynx (see below).<br />
Although all measures of <strong>cranial</strong> <strong>base</strong> angle<br />
are similar in that they attempt to quantify<br />
the overall degree of angulation in the<br />
midsagittal plane between the prechordal<br />
<strong>and</strong> postchordal portions of the <strong>cranial</strong> <strong>base</strong>,<br />
there have been at least 17 different measurements<br />
used since Huxley (1867) first<br />
attempted to quantify the angle (reviewed<br />
in Lieberman <strong>and</strong> McCarthy, 1999, <strong>and</strong><br />
summarized in Table 1). Many of these angles<br />
differ considerably in how they measure<br />
the prechordal <strong>and</strong> postchordal planes<br />
<strong>and</strong>, consequently, the point of intersection<br />
between them. Figure 5 illustrates some of<br />
these angles. <strong>The</strong> postchordal plane is most<br />
commonly defined using two l<strong>and</strong>marks,<br />
usually basion <strong>and</strong> sella, or using the line<br />
created by the dorsal surface of the basioccipital<br />
clivus (the clival line). <strong>The</strong> prechordal<br />
plane has been measured in more<br />
diverse ways. Historically, the most common<br />
plane is defined by two l<strong>and</strong>marks,<br />
sella <strong>and</strong> nasion. <strong>The</strong> sella-nasion line is<br />
problematic, however, because nasion is actually<br />
part of the face <strong>and</strong> moves anteriorly<br />
<strong>and</strong> inferiorly relative to the <strong>cranial</strong> <strong>base</strong><br />
throughout the period of facial growth<br />
(Scott, 1958; Enlow, 1990). Recently, most<br />
researchers have defined the prechordal<br />
plane either from sella to the foramen caecum<br />
(a pit on the anterior end of the cribriform<br />
plate between the crista galli between<br />
frontal squama), or using the planum sphenoideum<br />
which extends from sphenoidale<br />
(the most postero-superior point on the tuberculum<br />
sellae) to the planum sphenoideum<br />
point (defined as the most anterior<br />
point on the surface of the midline anterior
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 127<br />
TABLE 1. Commonly used measures of midsagittal <strong>cranial</strong> <strong>base</strong> angle<br />
Angle<br />
Posterior (P) <strong>and</strong> anterior (A)<br />
planes used<br />
References<br />
External <strong>cranial</strong> <strong>base</strong> angle P: basion-sella Björk, 1951, 1955; Stamrud, 1959<br />
Nasion-sella-basion A: sella-nasion Melsen, 1969; George, 1978<br />
L<strong>and</strong>zert’s sphenoidal angle<br />
Clivus/clival angle<br />
CBA4, planum angle<br />
P: clival plane<br />
A: ethmoidal plane (planum<br />
sphenoideum/ale)<br />
Clivus angle P: clival plane George, 1978<br />
A: sphenoidale-fronton<br />
Ethmoidal angle P: basion-sella Stamrud, 1959<br />
L<strong>and</strong>zert, 1866; Biegert, 1957;<br />
Moss, 1958; Hofer, 1957;<br />
Angst, 1967; Cartmill, 1970;<br />
Dmoch, 1975; Ross <strong>and</strong><br />
Ravosa, 1993; Ross <strong>and</strong><br />
Henneberg, 1995<br />
Internal <strong>cranial</strong> <strong>base</strong> angle<br />
A: sella-ethmoidale<br />
Spheno-ethmoidal angle P: basion-prosphenion Huxley, 1867; Topinard, 1890;<br />
Duckworth, 1904; Cameron,<br />
1924; Zuckerman, 1955<br />
Cameron’s cranio-facial axis<br />
P: basion-pituitary point<br />
A: pituitary point-nasion<br />
Cameron, 1924, 1925, 1927a,b,<br />
1930<br />
Basioccipito-septal angle P: basion-pituitary point Ford, 1956<br />
A: pituitary point-septal point<br />
Bolton’s external <strong>cranial</strong> <strong>base</strong> angle P: Bolton point-sella<br />
Brodie, 1941, 1953<br />
A: sella-nasion<br />
Anterior <strong>cranial</strong> <strong>base</strong> angle P: clival plane Scott, 1958; Cramer, 1977<br />
A: prosphenion-anterior cribriform<br />
point (ACP)<br />
Internal <strong>cranial</strong> <strong>base</strong> angle, basionsphenoidale-fronton<br />
Internal <strong>cranial</strong> <strong>base</strong> angle, basionsella-fronton<br />
Internal <strong>cranial</strong> <strong>base</strong> angle, basionsella-foramen<br />
caecum CBA1<br />
P: basion-sphenoidale<br />
A: sphenoidale-fronton<br />
P: basion-sella<br />
A: sella-fronton<br />
P: basion-sella<br />
A: sella-foramen caecum<br />
George, 1978<br />
George, 1978<br />
External <strong>cranial</strong> <strong>base</strong> angle, nasionsphenoidale-basion<br />
P: basion-sphenoidale<br />
A: sphenoidale-nasion<br />
Orbital angle P: clival plane Moss, 1958<br />
A: plane of superior orbital roof<br />
Planum angle (PANG) P: basion-sella Antón, 1989<br />
A: planum sphenoidale<br />
Orbital angle (OANG) P: basion-sella Antón, 1989<br />
A: plane of superior orbital roof<br />
Cousin et al., 1981; Spoor, 1997<br />
Lieberman <strong>and</strong> McCarthy,<br />
1999<br />
George, 1978<br />
<strong>cranial</strong> <strong>base</strong> posterior to the cribriform<br />
plate).<br />
Since different lines emphasize different<br />
aspects of <strong>cranial</strong> <strong>base</strong> anatomy, the choice<br />
of which <strong>cranial</strong> <strong>base</strong> angle to use is largely<br />
dependent on the question under study.<br />
Both postchordal lines tend to yield roughly<br />
similar results (George, 1978; Lieberman<br />
<strong>and</strong> McCarthy, 1999), but the prechordal<br />
lines can be substantially different. In particular,<br />
S-FC spans the entire length of the<br />
anterior <strong>cranial</strong> <strong>base</strong>, including the cribriform<br />
plate, whereas the planum sphenoideum<br />
does not measure the portion of the<br />
<strong>cranial</strong> <strong>base</strong> that includes the cribriform<br />
plate. Because of variation in the growth<br />
<strong>and</strong> position of the cribriform plate, these<br />
differences affect comparisons of anthropoids<br />
with strepsirrhines, or comparisons of<br />
<strong>primate</strong>s with other mammals (McCarthy,<br />
in press). In humans <strong>and</strong> some anthropoids,<br />
the cribriform plate lies in approximately<br />
the same plane as the planum sphenoideum,<br />
but in other anthropoids the cribriform<br />
plate lies in a deep olfactory pit within<br />
the ethmoidal notch of the frontal bone (Fig.<br />
6) (Aiello <strong>and</strong> Dean, 1990; Ravosa <strong>and</strong> Shea,<br />
1994). Moreover, in strepsirrhines <strong>and</strong><br />
other mammals with more divergent orbits<br />
<strong>and</strong> projecting snouts, the cribriform plate<br />
typically lies at a steep angle relative to the<br />
planum sphenoideum (Cartmill, 1970).<br />
Variations in <strong>cranial</strong> <strong>base</strong> angulation<br />
need to be considered in both comparative<br />
<strong>and</strong> ontogenetic studies. For example, it is<br />
well known that humans have a much more<br />
flexed <strong>cranial</strong> <strong>base</strong> than other <strong>primate</strong>s, but<br />
it is not well appreciated that the human
128 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Fig. 5. Major <strong>cranial</strong> <strong>base</strong> angles used in this review, illustrated in a human cranium. CBA1 is the<br />
angle between the basion-sella (Ba-S) line <strong>and</strong> the sella-foramen (S-FC) caecum line. CBA4 is the angle<br />
between the midline of the postclival plane, <strong>and</strong> the midline of the planum sphenoideum.<br />
Fig. 6. Lateral radiographs of hemisected baboon cranium (A) <strong>and</strong> human cranium (B). Note different<br />
orientation <strong>and</strong> position of the cribriform plate (CP) relative to the planum sphenoideum (PS) in the two<br />
species.<br />
<strong>cranial</strong> <strong>base</strong> flexes postnatally, while the<br />
nonhuman <strong>primate</strong> <strong>cranial</strong> <strong>base</strong> extends<br />
postnatally, possibly at different locations<br />
(Hofer, 1960; Sirianni <strong>and</strong> Swindler, 1979;<br />
Cousin et al., 1981; Lieberman <strong>and</strong> Mc-<br />
Carthy, 1999). <strong>The</strong>se potentially nonhomologous<br />
differences exist because changes<br />
in the <strong>cranial</strong> <strong>base</strong> angle can occur through<br />
different growth processes (e.g., drift, displacement)<br />
at different locations. <strong>The</strong> actual<br />
cellular processes that result in angulation,<br />
however, are not completely understood.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 129<br />
Some researchers (Scott, 1958; Giles et al.,<br />
1981; Enlow, 1990) suggest that changes in<br />
<strong>cranial</strong> <strong>base</strong> angulation occur interstitially<br />
within synchondroses through a hinge-like<br />
action. If so, flexion would result from increased<br />
chrondrogenic activity in the superior<br />
vs. inferior aspect of the synchondrosis,<br />
while extension would result from increased<br />
chrondrogenic activity in the inferior vs. superior<br />
aspect of the synchondrosis. Experimental<br />
growth studies in macaques, which<br />
labeled growth using flurochrome dyes,<br />
show that angulation also occurs through<br />
drift in which depository <strong>and</strong> resorptive<br />
growth fields differ on either side of a synchondrosis,<br />
causing rotations around an<br />
axis through the synchondrosis (Michejda,<br />
1971, 1972a; Michejda <strong>and</strong> Lamey, 1971;<br />
Giles et al., 1981). All three synchondroses<br />
are involved in prenatal angulation (Hofer,<br />
1960; Hofer <strong>and</strong> Spatz, 1963; Sirianni <strong>and</strong><br />
Newell-Morris, 1980; Diewert, 1985; Anagastopolou<br />
et al., 1988; Sperber, 1989; van<br />
den Eynde et al., 1992); however, the extent<br />
to which each synchondrosis participates in<br />
postnatal flexion <strong>and</strong> extension is poorly<br />
known, <strong>and</strong> probably differs between humans<br />
<strong>and</strong> nonhuman <strong>primate</strong>s. <strong>The</strong> SOS,<br />
which remains active until after the eruption<br />
of the second permanent molars, is<br />
probably the most active synchondrosis in<br />
generating angulation in <strong>primate</strong>s (Björk,<br />
1955; Scott, 1958; Melsen, 1969). <strong>The</strong> MSS<br />
fuses prior to birth in humans (Ford, 1958),<br />
but may also be important in nonhuman<br />
<strong>primate</strong>s (Scott, 1958; Hofer <strong>and</strong> Spatz,<br />
1963; Michejda, 1971, 1972a; but see Lager,<br />
1958; Melsen, 1971; Giles et al., 1981). Finally,<br />
the SES fuses near birth in nonhuman<br />
<strong>primate</strong>s, <strong>and</strong> remains active only as a<br />
site of <strong>cranial</strong> <strong>base</strong> elongation in humans<br />
during the neural growth period (Scott,<br />
1958; Michejda <strong>and</strong> Lamey, 1971). Other<br />
ontogenetic changes in the <strong>cranial</strong> <strong>base</strong> angle<br />
(not necessarily involved in angulation<br />
itself) include posterior drift of the foramen<br />
magnum (see above), inferior drift of the<br />
cribriform plate relative to the anterior <strong>cranial</strong><br />
<strong>base</strong> (Moss, 1963), <strong>and</strong> remodeling of<br />
the sella turcica, which causes posterior<br />
movement of the sella (Baume, 1957; Shapiro,<br />
1960; Latham, 1972).<br />
A few experimental studies provide evidence<br />
for the presence of complex interactions<br />
between the brain <strong>and</strong> <strong>cranial</strong> <strong>base</strong><br />
synchondroses that influence variation in<br />
the <strong>cranial</strong> <strong>base</strong> angle. DuBrul <strong>and</strong> Laskin<br />
(1961), Moss (1976), Bütow (1990), <strong>and</strong> Reidenberg<br />
<strong>and</strong> Laitman (1991) all inhibited<br />
growth in the SOS in various animals<br />
(mostly rats), causing a more flexed <strong>cranial</strong><br />
<strong>base</strong>, presumably through inhibition of <strong>cranial</strong><br />
<strong>base</strong> extension. In most of these studies,<br />
experimentally induced kyphosis of the<br />
basicranium was also associated with a<br />
shorter posterior portion of the <strong>cranial</strong> <strong>base</strong>,<br />
<strong>and</strong> a more rounded neurocranium (see below).<br />
Artificial deformation of the <strong>cranial</strong><br />
vault also causes slight but significant increases<br />
in <strong>cranial</strong> <strong>base</strong> angulation (Antón,<br />
1989; Kohn et al., 1993). However, no controlled<br />
experimental studies have yet examined<br />
disruptions to the other <strong>cranial</strong> <strong>base</strong><br />
synchondroses. In addition, there have been<br />
few controlled studies of the effect of increasing<br />
brain size on <strong>cranial</strong> <strong>base</strong> angulation.<br />
In one classic experiment, Young<br />
(1959) added sclerosing fluid into the <strong>cranial</strong><br />
cavity in growing rats, which caused<br />
enlargement of the neurocranium with little<br />
effect on angular relationships in the <strong>cranial</strong><br />
<strong>base</strong>. Additional evidence for some degree<br />
of independence between the brain <strong>and</strong><br />
<strong>cranial</strong> <strong>base</strong> during development is provided<br />
by microcephaly <strong>and</strong> hydrocephaly, in<br />
which <strong>cranial</strong> <strong>base</strong> angles tend to be close to<br />
those of humans with normal encephalization<br />
(Moore <strong>and</strong> Lavelle, 1974; Sperber,<br />
1989).<br />
Important differences in <strong>cranial</strong> <strong>base</strong> angulation<br />
among <strong>primate</strong>s exist in terms of<br />
the ontogenetic pattern of flexion <strong>and</strong>/or extension,<br />
which presumably result from differences<br />
in the rate, timing, duration, <strong>and</strong><br />
sequence of the growth processes outlined<br />
above. Jeffery (1999) suggested that, prenatally,<br />
the basicranium in humans initially<br />
flexes rapidly during the period of rapid<br />
hindbrain growth in the first trimester, remains<br />
fairly stable during the second trimester,<br />
<strong>and</strong> then extends during the third<br />
trimester in conjunction with facial extension,<br />
even while the brain is rapidly increasing<br />
in size relative to the rest of the cranium<br />
(see also Björk, 1955; Ford, 1956; Sperber,
130 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Fig. 7. Changes in the angle of the <strong>cranial</strong> <strong>base</strong> (CBA1 <strong>and</strong> CBA4) in Homo sapiens (left) <strong>and</strong> Pan<br />
troglodytes (right) (after Fig. 6 in Lieberman <strong>and</strong> McCarthy, 1999). For both species, means (circles) <strong>and</strong><br />
st<strong>and</strong>ard deviations (whiskers) are summarized by the mean chronological age of each dental stage. Note<br />
that the human <strong>cranial</strong> <strong>base</strong> flexes rapidly during stage I <strong>and</strong> then remains stable, whereas the<br />
chimpanzee <strong>cranial</strong> <strong>base</strong> extends gradually through stage V. *P 0.05.<br />
1989; van den Eynde et al., 1992). Little is<br />
known about prenatal <strong>cranial</strong> <strong>base</strong> angulation<br />
in nonhuman <strong>primate</strong>s; however, major<br />
differences between humans <strong>and</strong> nonhumans<br />
appear during the fetal <strong>and</strong> postnatal<br />
periods of growth. As Figure 7 illustrates,<br />
the human <strong>cranial</strong> <strong>base</strong> flexes rapidly after<br />
birth, almost entirely prior to 2 years of age,<br />
<strong>and</strong> well before the brain has ceased to exp<strong>and</strong><br />
appreciably (Lieberman <strong>and</strong> Mc-<br />
Carthy, 1999). In contrast, the nonhuman<br />
<strong>primate</strong> <strong>cranial</strong> <strong>base</strong> extends gradually after<br />
birth throughout the neural <strong>and</strong> facial<br />
growth periods, culminating in an accelerated<br />
phase during the adolescent growth<br />
spurt (Hofer, 1960; Heintz, 1966; Sirianni<br />
<strong>and</strong> Swindler, 1979; Cousin et al., 1981;<br />
Lieberman <strong>and</strong> McCarthy, 1999).<br />
<strong>The</strong> polyphasic <strong>and</strong> multifactorial nature<br />
of <strong>cranial</strong> <strong>base</strong> angulation during <strong>ontogeny</strong><br />
<strong>and</strong> the ontogenetic contrasts between the<br />
relative contribution of underlying factors<br />
in humans <strong>and</strong> nonhumans provide some<br />
clues for underst<strong>and</strong>ing the complex, multiple<br />
interactions between <strong>cranial</strong> <strong>base</strong> angulation,<br />
encephalization, <strong>and</strong> facial growth.<br />
<strong>The</strong>re is abundant evidence <strong>base</strong>d on interspecific<br />
studies (see below) that variation in<br />
<strong>cranial</strong> <strong>base</strong> angle in <strong>primate</strong>s is associated<br />
in part with variation in brain volume relative<br />
to the length of the <strong>cranial</strong> <strong>base</strong>. However,<br />
relative encephalization accounts for<br />
only 36% of the variation in <strong>cranial</strong> <strong>base</strong><br />
angle among anthropoids, <strong>and</strong> both interspecific<br />
<strong>and</strong> ontogenetic data suggest that a<br />
large proportion of the variation in <strong>cranial</strong>
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 131<br />
<strong>base</strong> angle among <strong>primate</strong>s must also be<br />
related to variation in facial growth, orbit<br />
orientation, <strong>and</strong> relative orbit size (Ross <strong>and</strong><br />
Ravosa, 1993; Ravosa et al., 2000a). As<br />
noted above, the ontogenetic pattern of prenatal<br />
<strong>cranial</strong> <strong>base</strong> angulation in humans is<br />
largely unrelated to the rate at which the<br />
brain exp<strong>and</strong>s (Jeffery, 1999). In addition,<br />
the nonhuman <strong>primate</strong> <strong>cranial</strong> <strong>base</strong> angle<br />
(regardless of whether the cribriform plate<br />
is included in the measurement) mostly extends<br />
during the period of facial growth,<br />
after the brain has ceased to exp<strong>and</strong><br />
(Lieberman <strong>and</strong> McCarthy, 1999). <strong>The</strong>refore,<br />
we will next explore in greater depth<br />
the relationship between <strong>cranial</strong> <strong>base</strong> angle,<br />
brain size, relative orbit size <strong>and</strong> position,<br />
facial orientation, <strong>and</strong> other factors such as<br />
pharyngeal shape <strong>and</strong> facial projection.<br />
ASSOCIATIONS BETWEEN CRANIAL<br />
BASE AND BRAIN<br />
Because of the close relationship between<br />
the brain <strong>and</strong> the <strong>cranial</strong> <strong>base</strong> during development<br />
(see above), the hypothesis that<br />
brain size <strong>and</strong> shape influence basi<strong>cranial</strong><br />
morphology is an old <strong>and</strong> persistent one.<br />
<strong>The</strong> bones of the <strong>cranial</strong> cavity, including<br />
the <strong>cranial</strong> <strong>base</strong>, are generally known to<br />
conform to the shape of the brain, but the<br />
specifics of this relationship <strong>and</strong> any reciprocal<br />
effects of <strong>cranial</strong> <strong>base</strong> size <strong>and</strong> shape<br />
on brain morphology remain unclear. For<br />
example, the human basicranium is flexed<br />
when it first appears in weeks 5 <strong>and</strong> 6 because<br />
in the fourth week, the neural tube<br />
bends ventrally at the cephalic flexure<br />
(O’Rahilly <strong>and</strong> Müller, 1994). <strong>The</strong> parachordal<br />
condensations caudal to the cephalic<br />
flexure are therefore in a different<br />
anatomical plane than the more rostral prechordal<br />
condensations (which develop by<br />
week 7). However, as noted above, it is difficult<br />
to attribute many of the subsequent<br />
changes in prenatal chondro<strong>cranial</strong> or basi<strong>cranial</strong><br />
angulation (or other measures of the<br />
<strong>base</strong>) as responses solely to changes in brain<br />
morphology.<br />
Here we review several key aspects of the<br />
association between brain <strong>and</strong> <strong>cranial</strong> <strong>base</strong><br />
morphology, as derived from interspecific<br />
analyses of adult specimens. Structural relationships<br />
between the <strong>cranial</strong> <strong>base</strong> <strong>and</strong><br />
the face are discussed below.<br />
Brain size <strong>and</strong> <strong>cranial</strong> <strong>base</strong> angle<br />
Numerous anatomists have posited a relationship<br />
between brain size <strong>and</strong> basi<strong>cranial</strong><br />
angle (e.g., Virchow, 1857; Ranke, 1892;<br />
Cameron, 1924; Bolk, 1926; Dabelow, 1929,<br />
1931; Biegert, 1957, 1963; Delattre <strong>and</strong> Fenart,<br />
1963; Hofer, 1969; Gould, 1977; Ross<br />
<strong>and</strong> Ravosa, 1993; Ross <strong>and</strong> Henneberg,<br />
1995; Spoor, 1997; Strait, 1999; Strait <strong>and</strong><br />
Ross, 1999; McCarthy, 2001). <strong>The</strong> most<br />
widely accepted of these hypotheses is that<br />
the angle of the midline <strong>cranial</strong> <strong>base</strong> in the<br />
sagittal plane correlates with the volume of<br />
the brain relative to basi<strong>cranial</strong> length<br />
(DuBrul <strong>and</strong> Laskin, 1961; Vogel, 1964;<br />
Riesenfeld, 1969; Gould, 1977). This hypothesis<br />
is supported by independent analyses of<br />
different measures of basi<strong>cranial</strong> flexion<br />
across several interspecific samples of <strong>primate</strong>s<br />
(Ross <strong>and</strong> Ravosa, 1993; Spoor, 1997;<br />
McCarthy, 2001) (Fig. 8): the adult midline<br />
<strong>cranial</strong> <strong>base</strong> is significantly <strong>and</strong> predictably<br />
more flexed in species with larger endo<strong>cranial</strong><br />
volumes relative to basi<strong>cranial</strong> length.<br />
In particular, the analysis by Ross <strong>and</strong> Ravosa<br />
(1993) of a broad interspecific sample<br />
of <strong>primate</strong>s found that the correlation coefficient<br />
between relative encephalization<br />
(IRE1, see below) <strong>and</strong> <strong>cranial</strong> <strong>base</strong> angle<br />
(CBA4, see below) was 0.645 (P 0.001),<br />
explaining approximately 40% of the variation<br />
in <strong>cranial</strong> <strong>base</strong> angle.<br />
Attempts to extend this relationship to<br />
hominins have proved controversial. Ross<br />
<strong>and</strong> Henneberg (1995) reported that Homo<br />
sapiens have less flexed basicrania than<br />
predicted by either haplorhine or <strong>primate</strong><br />
regressions. <strong>The</strong>y posited that spatial constraints<br />
limit the degree of flexion possible,<br />
<strong>and</strong> that humans accommodate further<br />
brain expansion relative to <strong>cranial</strong> <strong>base</strong><br />
length through means other than flexion,<br />
such as superior, posterior, <strong>and</strong> lateral neuro<strong>cranial</strong><br />
expansion. In contrast, Spoor<br />
(1997), using different measures of flexion<br />
<strong>and</strong> relative brain size taken on a different<br />
sample, found H. sapiens to have the degree<br />
of flexion expected for its relative brain size.<br />
Spoor (1997) used the angle basion-sellaforamen<br />
caecum (CBA1) to quantify basi-
132 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Fig. 8. Bivariate plot of CBA4 against IRE5. <strong>The</strong>se variables are significantly correlated across<br />
Primates (r 0.621; P 0.05) <strong>and</strong> Haplorhini (r 0.636; P 0.05).<br />
<strong>cranial</strong> flexion, <strong>and</strong> the length of these line<br />
segments (thereby including cribriform<br />
plate length) to quantify basi<strong>cranial</strong> length<br />
(BL2), whereas Ross <strong>and</strong> Henneberg (1995)<br />
measured flexion using CBA4 <strong>and</strong> relative<br />
brain size using IRE1 (endo<strong>cranial</strong> volume<br />
0.33 /BL1).<br />
<strong>The</strong> two most likely sources of the discrepancy<br />
between the results of Spoor (1997) vs.<br />
Ross <strong>and</strong> Henneberg (1995) were the different<br />
measures <strong>and</strong> different samples. Mc-<br />
Carthy (2001) has since investigated the influence<br />
of different measures, noting that<br />
the measure of basi<strong>cranial</strong> length by Ross<br />
<strong>and</strong> Henneberg (1995) excluded the horizontally<br />
oriented cribriform plate that contributes<br />
to basi<strong>cranial</strong> length in anthropoids<br />
more than in strepsirrhines. McCarthy<br />
(2001) also demonstrated that the frontal<br />
bone contributes less to midline <strong>cranial</strong> <strong>base</strong><br />
length in hominoids, especially humans,<br />
causing BL1 to underestimate midline basi<strong>cranial</strong><br />
length relative to endo<strong>cranial</strong> volume<br />
compared to other anthropoids. However,<br />
the data sets of both McCarthy (2000)<br />
<strong>and</strong> Spoor (1997) were small (n 17 species)<br />
in comparison with that of Ross <strong>and</strong><br />
Henneberg (1995) (n 64 species). We<br />
therefore reanalyzed the relationships between<br />
flexion <strong>and</strong> relative brain size in a<br />
large interspecific <strong>primate</strong> sample, utilizing<br />
both CBA1 <strong>and</strong> CBA4 as measures of flexion<br />
<strong>and</strong> IRE5 as a measure of relative brain<br />
size. 2 IRE5 incorporates the more appropriate<br />
basi<strong>cranial</strong> length that includes cribriform<br />
plate length (see Glossary <strong>and</strong> Measurement<br />
Definitions). <strong>The</strong> human value for<br />
CBA1 falls within the 95% confidence limits<br />
of the value predicted for an anthropoid of<br />
its relative brain size, but the human value<br />
for CBA4 does not. <strong>The</strong>se results corroborate<br />
those of McCarthy (2001): the degree of<br />
basi<strong>cranial</strong> flexion in humans is not significantly<br />
less than expected using CBA1, but<br />
is less than expected using CBA4. Thus humans<br />
may or may not have the degree of<br />
2 Measurements were taken on radiographs of nonhuman <strong>primate</strong>s<br />
from Ravosa (1991b) <strong>and</strong> Ross <strong>and</strong> Ravosa (1993), <strong>and</strong> on<br />
98 Homo sapiens from Ross <strong>and</strong> Henneberg (1995). RMA slopes<br />
were calculated for nonhominin <strong>primate</strong>s, <strong>and</strong> the 95% bootstrap<br />
confidence limits for the value of y predicted for humans were<br />
calculated according to Joliceur <strong>and</strong> Mosiman (1968), using software<br />
written by Tim Cole.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 133<br />
TABLE 2. Variance components for indices of relative brain size <strong>and</strong> measures of flexion across <strong>primate</strong>s 1<br />
Level<br />
N<br />
IRE1 IRE5 CBA4 CBA1<br />
% N eff % N eff % N eff % N eff<br />
Infraorder 2 12 0.24 48 0.94 0 0 52 1.05<br />
Superfamily 6 22 1.34 10 0.62 34 2.07 0 0.00<br />
Family 15 54 8.16 16 2.44 44 6.56 35 5.19<br />
Genus 60 13 7.81 22 12.99 17 10.26 8 4.74<br />
Species 62 1 0.78 3 2.38 5 3.10 5 3.25<br />
Total N eff 18.33 17.38 21.99 14.23<br />
df 16.00 15.00 20.00 12.00<br />
1 Maximum likelihood variance components were calculated using mainframe SAS (proc varcomp). %, percentage of variance at<br />
each taxonon 1 mic level; N eff , effective N at each level; Total N eff , total effective N for each variable. Bivariate comparisons utilize<br />
lowest N eff of the pair.<br />
TABLE 3. Correlation coefficients for <strong>primate</strong>s <strong>and</strong> haplorhini 1<br />
Variables CBA4 N (P) df eff (P) CBA1 N (P) df eff (P)<br />
Primates<br />
IRE1 0.783 60 (0.001) 14 (0.01) 0.672 60 (0.001) 10 (0.05)<br />
IRE5 0.621 60 (0.001) 13 (0.05) 0.790 62 (0.001) 10 (0.01)<br />
Haplorhini<br />
IRE1 0.813 51 (0.001) 9 (0.01) 0.641 51 (0.001) 9 (0.05)<br />
IRE5 0.636 51 (0.001) 10 (0.05) 0.548 51 (0.001) 14 (0.05)<br />
1 N, total N; d eff ,N eff 2, effective degrees of freedom for each comparison. Bivariate comparisons utilize lowest N eff of the pair.<br />
flexion expected for their relative brain size,<br />
depending on which measures are used.<br />
One problem with the above studies is<br />
that they do not consider the potential role<br />
of phylogenetic effects on these correlations<br />
(Cheverud et al., 1985; Felsenstein, 1985).<br />
Accordingly, the above data were reanalyzed<br />
using the method of Smith (1994) for<br />
adjusting degrees of freedom. 3 Table 2 presents<br />
the percentage of total variance distributed<br />
at each taxonomic level within the<br />
order Primates. Table 3 presents the correlation<br />
coefficients for comparisons of CBA<br />
<strong>and</strong> IRE for Primates <strong>and</strong> Haplorhini, along<br />
with sample sizes, degrees of freedom adjusted<br />
for phylogeny (df eff ), <strong>and</strong> their associated<br />
P-values (for which strepsirrhines<br />
had no significant correlations). Examination<br />
of the variance components in Table 2<br />
shows that the relationship between <strong>cranial</strong><br />
<strong>base</strong> angle <strong>and</strong> relative brain size is subject<br />
to significant phylogenetic effects. However,<br />
3 Unlike methods such as “independent contrasts” (e.g., Purvis<br />
<strong>and</strong> Rambaut, 1995), Smith’s method uses values for variables in<br />
just terminal taxa, therefore avoiding potentially spurious estimates<br />
of these values for ancestral nodes. Smith’s method is also<br />
more robust when five or fewer taxonomic levels are considered<br />
<strong>and</strong> is less affected by arbitrary taxonomic groupings (Nunn,<br />
1995). We also used the maximum likelihood method for calculating<br />
variance components rather than a nested ANOVA<br />
method because maximum likelihood does not generate negative<br />
variance components.<br />
the method of Smith (1994) is conservative<br />
<strong>and</strong> the correlations that survive these corrected<br />
degrees of freedom are robust, although<br />
of relatively low magnitude. Across<br />
<strong>primate</strong>s <strong>and</strong> haplorhines, both CBA4 <strong>and</strong><br />
CBA1 are significantly correlated (P 0.05)<br />
with IRE5 (Fig. 8; Table 2). <strong>The</strong>se results<br />
corroborate the results of Ross <strong>and</strong> Ravosa<br />
(1993), but with a more appropriate measure<br />
of basi<strong>cranial</strong> length incorporated into<br />
the measure of relative brain size. This confirms<br />
that brain size relative to basi<strong>cranial</strong><br />
length is significantly correlated with basi<strong>cranial</strong><br />
flexion, but that the correlations are<br />
not particularly strong, indicating that<br />
there may be other important influences on<br />
the degree of basi<strong>cranial</strong> flexion (see below).<br />
Most hypotheses explaining basi<strong>cranial</strong><br />
flexion have focused on increases in relative<br />
brain size as the variable driving flexion.<br />
However, as Strait (1999) has noted, it is<br />
important to consider the scaling relationships<br />
of basi<strong>cranial</strong> length <strong>and</strong> brain size.<br />
Using interspecific data from Ross <strong>and</strong> Ravosa<br />
(1993) in conjunction with other studies,<br />
Strait (1999) found that basi<strong>cranial</strong><br />
length scales with negative allometry<br />
against body mass <strong>and</strong> telencephalon volume<br />
(results confirmed here using BL2 instead<br />
of BL1; see Table 4), <strong>and</strong> BL2 also
134 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
TABLE 4. Reduced major axis regression equations for scaling of basi<strong>cranial</strong> dimensions against<br />
neural variables 1<br />
Comparison Intercept Slope<br />
95% CI<br />
of slope Scaling 3 N r<br />
BL2 vs.<br />
Body mass 0.908 0.654 0.035 ve 61 0.978<br />
Telencephalon 0.541 0.742 0.091 ve 33 0.960<br />
Brain stem 0.404 1.123 0.100 ve/Iso 33 0.975<br />
Neuro<strong>cranial</strong> volume 1.270 0.734 0.056 ve 62 0.962<br />
Palate (Pros-PNS) 1.394 0.642 0.032 ve 58 0.929<br />
Anterior face (Pros-Nas) 1.623 0.577 0.028 ve 58 0.933<br />
Upper toothroow 1.425 0.666 0.035 ve 58 0.921<br />
Geometric mean 2 0.951 0.750 0.023 ve 58 0.972<br />
Ba-S vs.<br />
Body mass 0.380 0.759 0.056 ve 63 0.958<br />
Brain stem 0.226 1.354 0.161 ve 33 0.946<br />
Telencephalon 0.313 0.908 0.135 Iso 33 0.924<br />
Cerebellum 0.105 0.953 0.111 Iso 33 0.948<br />
Infratentorial brain 0.064 1.044 0.123 Iso 33 0.947<br />
Palate (Pros-PNS) 0.595 0.757 0.040 ve 58 0.917<br />
Anterior face (Pros-Nas) 0.862 0.681 0.037 ve 58 0.914<br />
Upper toothroow 0.626 0.787 0.043 ve 58 0.924<br />
Geometric mean 2 0.067 0.886 0.034 ve 58 0.957<br />
S-FC vs.<br />
Ba-S 0.473 0.759 0.063 ve 33 0.949<br />
Body mass 0.748 0.587 0.040 ve 56 0.965<br />
Brain stem 0.249 1.070 0.101 Iso 33 0.971<br />
Telencephalon 0.378 0.715 0.082 ve 33 0.963<br />
Cerebellum 0.516 0.749 0.079 ve 33 0.964<br />
Infratentorial brain 0.381 0.822 0.085 ve 33 0.965<br />
Palate (Pros-PNS) 1.382 0.581 0.032 ve 58 0.912<br />
Anterior face (Pros-Nas) 1.586 0.523 0.027 ve 58 0.922<br />
Upper toothroow 1.406 0.604 0.035 ve 58 0.900<br />
Geometric mean 2 0.977 0.680 0.026 ve 58 0.958<br />
1 All volumetric <strong>and</strong> mass variables converted to cube roots. All calculations in log-log space (<strong>base</strong> 10). Calculations with facial<br />
dimensions do not include humans; all other calculations include humans.<br />
2 Geometric mean of the following measures: palate length, palate breadth, anterior face length, maxillary postcanine toothrow<br />
length, outer biorbital breadth, bizygomatic breadth, basi<strong>cranial</strong> length, <strong>and</strong> lower skull length. Measures of brain volume from<br />
Stephan et al. (1981), measures of body mass from Smith <strong>and</strong> Jungers (1994), <strong>and</strong> measures of facial size derive from the same skulls<br />
from which the radiographs were taken.<br />
3 ve, negative; ve, positive; Iso, isometric.<br />
scales with negative allometry against measures<br />
of facial size (Table 4). <strong>The</strong> only variable<br />
that scales close to isometry with basi<strong>cranial</strong><br />
length is brain-stem volume, which<br />
is isometric with BL1 <strong>and</strong> scales close to<br />
isometry with BL2 (Table 4). Intuitively this<br />
isometry makes sense, because the brain<br />
stem rests on the basicranium. However,<br />
the posterior basicranium (Ba-S), which<br />
predominantly underlies the brain stem,<br />
scales with positive allometry to brain-stem<br />
volume, whereas the anterior <strong>cranial</strong> <strong>base</strong><br />
length scales isometrically with brain-stem<br />
volume. Notably, the anterior <strong>cranial</strong> <strong>base</strong><br />
always shows lower slopes than the posterior<br />
<strong>cranial</strong> <strong>base</strong>, suggesting that the strong<br />
negative allometry of <strong>cranial</strong> <strong>base</strong> length<br />
relative to neural variables, <strong>and</strong> possibly<br />
flexion, is disproportionately attributable to<br />
relative shortening of the anterior <strong>cranial</strong><br />
<strong>base</strong>.<br />
Brain shape <strong>and</strong> <strong>cranial</strong> <strong>base</strong> angle<br />
Given the close anatomical relationship<br />
between the brain <strong>and</strong> basicranium, it<br />
seems intuitive that the shapes of the two<br />
should be related, but testing this hypothesis<br />
in a controlled fashion has been difficult.<br />
<strong>The</strong> best evidence for the presence of interactions<br />
between brain shape <strong>and</strong> the <strong>cranial</strong><br />
<strong>base</strong> came from studies of artificial <strong>cranial</strong><br />
vault deformation <strong>and</strong> from the effects of<br />
closing various <strong>cranial</strong> vault sutures on the<br />
<strong>cranial</strong> <strong>base</strong>. <strong>The</strong> effects of head-binding are<br />
difficult to interpret without precise data on<br />
the timing <strong>and</strong> forces used to deform the<br />
skull. Nevertheless, antero-posterior headbinding<br />
tends to cause lateral expansion of
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 135<br />
Fig. 9. Bivariate plot of the measure by Hofer (1969)<br />
of basi<strong>cranial</strong> flexion <strong>and</strong> CBA4 against his measure of<br />
brain flexion. Hofer’s brain angle is the anterior angle<br />
between Forel’s axis, from the most antero-inferior<br />
point on the frontal lobe to the most postero-inferior<br />
point on the occipital lobe, <strong>and</strong> Meynert’s axis, from the<br />
ventral edge of the junction between the pons <strong>and</strong> medulla<br />
to the caudal recess of the interpeduncular fossa.<br />
<strong>The</strong> data of Hofer (1969) measure anterior angles between<br />
lines, rather than the inferior angles favored by<br />
recent workers (e.g., Ross <strong>and</strong> Ravosa, 1993). <strong>The</strong> plotted<br />
data therefore represent the complement of Hofer’s<br />
angles.<br />
the <strong>cranial</strong> <strong>base</strong> along with a slight increase<br />
in CBA; conversely, annular head-binding<br />
tends to cause medio-lateral narrowing <strong>and</strong><br />
antero-posterior elongation of the <strong>cranial</strong><br />
<strong>base</strong>, also with a slight increase in CBA<br />
(Antón, 1989; Cheverud et al., 1992; Kohn et<br />
al., 1993). Natural or experimentally induced<br />
premature closure of sutures (synostoses)<br />
in the <strong>cranial</strong> vault have similarly<br />
predictable effects. For example, bilateral<br />
coronal synostoses cause antero-posterior<br />
shortening of the <strong>cranial</strong> <strong>base</strong> (Babler, 1989;<br />
David et al., 1989), <strong>and</strong> unilateral coronal<br />
synostoses (plagiocephaly) cause marked<br />
asymmetry in the <strong>cranial</strong> vault, <strong>cranial</strong><br />
<strong>base</strong>, <strong>and</strong> face.<br />
Interspecific analyses of the relationship<br />
between brain shape <strong>and</strong> <strong>cranial</strong> <strong>base</strong> shape<br />
in <strong>primate</strong>s are rare. Hofer (1965, 1969)<br />
measured the orientation of the cerebral<br />
hemispheres relative to the brain stem in<br />
<strong>primate</strong>s using two axes: Forel’s axis, from<br />
the most antero-inferior point on the frontal<br />
lobe to the most postero-inferior point on the<br />
occipital lobe, measuring the orientation of<br />
the inferior surface of the cerebral hemispheres;<br />
<strong>and</strong> Meynert’s axis, from the ventral<br />
edge of the junction between the pons<br />
<strong>and</strong> medulla to the caudal recess of the interpeduncular<br />
fossa, quantifying the orientation<br />
of the brain stem. Hofer (1965) also<br />
measured the angle of the midline <strong>cranial</strong><br />
<strong>base</strong> using a modified version of the angle of<br />
L<strong>and</strong>zert (1866), similar to the CBA4 used<br />
by Ross <strong>and</strong> Ravosa (1993).<br />
Figure 9, a plot of the measure by Hofer of<br />
basi<strong>cranial</strong> angle against his measure of<br />
brain angle, illustrates that these variables<br />
are highly correlated <strong>and</strong> scale isometrically<br />
with each other (i.e., have a slope of 1.0). As<br />
the cerebrum flexes on the brain stem, the<br />
planum sphenoideum flexes relative to the<br />
clivus. <strong>The</strong> explanation of Hofer (1969) for<br />
this phenomenon is that the telencephalon<br />
becomes more spherical as it enlarges, to<br />
minimize surface area relative to volume.<br />
An alternative hypothesis is that increasing<br />
the antero-posterior diameter of the head<br />
“would be disastrous, making larger animals<br />
unusually long-headed, <strong>and</strong> would pro-
136 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
TABLE 5. Correlation coefficients for flexion vs. measures of relative brain size<br />
N N eff (df) CBA4 CBA1<br />
Neocortex volume/BL2<br />
Primates 29 12 (10) 0.613 (0.05) 0.759 (0.01)<br />
Haplorhines 22 9 (7) 0.636 (ns) 0.660 (ns)<br />
Strepsirhines 7 6 (4) 0.282 (ns) 0.771 (ns)<br />
Telencephalon/brain-stem volume<br />
Primates 29 9 (7) 0.744 (0.05) 0.663 (ns)<br />
Haplorhines 19 6 (4) 0.726 (ns) 0.643 (ns)<br />
Strepsirhines 9 7 (5) 0.760 (0.05) 0.286 (ns)<br />
duce serious problems for balancing the<br />
skull on the skeleton” (Jerison, 1982, p. 82).<br />
In the context of such spatial constraints<br />
(i.e., limited cerebral diameter <strong>and</strong> tendency<br />
to sphericity), increased cerebrum size can<br />
only be accommodated by exp<strong>and</strong>ing the<br />
<strong>cranial</strong> <strong>base</strong> inferiorly, posteriorly, or anteriorly,<br />
thereby necessarily flexing the brain<br />
<strong>and</strong> the basicranium. <strong>The</strong> hypothesis of<br />
Jerison (1982) is refuted by animals such as<br />
camels, llamas, <strong>and</strong> giraffes, which have<br />
long heads on relatively orthograde necks;<br />
<strong>and</strong> as discussed below, there is no convincing<br />
evidence that head <strong>and</strong> neck posture are<br />
significant influences on basi<strong>cranial</strong> angle<br />
in <strong>primate</strong>s (Strait <strong>and</strong> Ross, 1999).<br />
Biegert (1963) made a claim similar to<br />
that of Hofer (1969), in arguing that increases<br />
in <strong>primate</strong> brain size relative to <strong>cranial</strong><br />
<strong>base</strong> size, as well as increases in “neopallium”<br />
(i.e., neocortex) size relative to<br />
other parts of the brain, produced a rounder<br />
brain such that “adaptations in the structure<br />
of the cranium accompanied these<br />
changes in the size <strong>and</strong> shape of the brain”<br />
(Biegert, 1963, p. 120). <strong>The</strong> predicted<br />
changes in skull shape include increased<br />
vaulting of the frontal <strong>and</strong> occipital bones<br />
<strong>and</strong> increased basi<strong>cranial</strong> flexion. Ross <strong>and</strong><br />
Ravosa (1993) evaluated the hypothesis of<br />
Biegert (1963) by calculating correlation coefficients<br />
between <strong>cranial</strong> <strong>base</strong> angle<br />
(CBA4) <strong>and</strong> the ratio of neocortical volume<br />
0.33 /basi<strong>cranial</strong> length. Although they<br />
found a significant relationship across <strong>primate</strong>s<br />
<strong>and</strong> haplorhines, the correlation coefficients<br />
were low (around 0.5). Recalculation<br />
of these correlation coefficients using BL2<br />
as a measure of basi<strong>cranial</strong> length produces<br />
significant correlations across <strong>primate</strong>s,<br />
haplorhines, <strong>and</strong> strepsirrhines, but only<br />
the <strong>primate</strong> level correlations survive adjusted<br />
degrees of freedom (Table 5).<br />
Strait (1999) proposed a hypothesis similar<br />
to those of Hofer (1969) <strong>and</strong> Biegert<br />
(1963). Noting that total basi<strong>cranial</strong> length<br />
scales close to isometry with noncortical<br />
brain volume, Strait (1999) suggested that<br />
variation in the midline basi<strong>cranial</strong> angle<br />
might be due to increases in the size of the<br />
telencephalon relative to the noncortical<br />
part of the brain, 4 rather than the size of the<br />
brain relative to the <strong>cranial</strong> <strong>base</strong>. Analysis<br />
of our data set confirms this hypothesis:<br />
there are significant correlations between<br />
flexion <strong>and</strong> the size of the telencephalon<br />
relative to the brain stem across <strong>primate</strong>s,<br />
using CBA4 (Table 5). Moreover, the only<br />
significant correlation between <strong>cranial</strong> <strong>base</strong><br />
angle <strong>and</strong> a neural variable among strepsirrhines<br />
is the comparison of CBA4 with the<br />
ratio of telencephalon to brain-stem volume<br />
(Table 5). However, despite relatively high<br />
correlation coefficients for haplorhines, these<br />
correlations do not remain significant with<br />
phylogenetically adjusted degrees of freedom.<br />
This suggests that brain size relative<br />
to basi<strong>cranial</strong> length may be a better explanation<br />
for flexion, because it appears to be<br />
more independent of phylogenetic effects.<br />
Whether basi<strong>cranial</strong> flexion accommodates<br />
increases in telencephalon volume relative<br />
to brain-stem volume, <strong>and</strong>/or increases<br />
in overall endo<strong>cranial</strong> volume<br />
relative to <strong>cranial</strong> <strong>base</strong> length, the end result<br />
is a change in brain shape. <strong>The</strong> enlarged<br />
telencephalon of <strong>primate</strong>s is an outgrowth<br />
of the rostral end of the brain stem<br />
that communicates with the rest of the<br />
brain through the diencephalon at its root.<br />
4 Strait (1999) refers to this as the “noncortical scaling hypothesis;”<br />
however, the telencephlon consists of more than cortex: it<br />
also includes the white matter <strong>and</strong> the basal ganglia. Here we<br />
evaluate the role of relative telencephalon volume in producing<br />
flexion.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 137<br />
Increasing the size of the outer cortex of the<br />
telencephalon (the neocortex) while still<br />
connecting to the rest of the brain through<br />
the diencephalon might be expected to generate<br />
a more spheroid shape, regardless of<br />
any <strong>function</strong>al constraints on skull or brain<br />
shape. In other words, the telencephalon<br />
may be spheroidal because of the geometry<br />
of its connections <strong>and</strong> the way it develops,<br />
rather than for any <strong>function</strong>al or adaptive<br />
reason. Alternately, a spheroidal cerebrum<br />
may minimize “wiring length” in the brain,<br />
a potentially important principle of design<br />
in neural architecture (Allman <strong>and</strong> Kaas,<br />
1974; Barlow, 1986; Mitchison, 1991; Cherniak,<br />
1995; Van Essen, 1997). Accordingly, a<br />
spheroid telencephalon may optimize neocortical<br />
wiring lengths as well as minimize<br />
the distance from all points in the cerebrum<br />
to the diencephalon, a structure through<br />
which all connections to the rest of the brain<br />
must pass (Ross <strong>and</strong> Henneberg, 1995). Another<br />
possible advantage of a flexed basicranium<br />
derives from the in vitro experiments<br />
of Demes (1985), showing that the angulation<br />
of the <strong>cranial</strong> <strong>base</strong> in combination with<br />
a spherical neurocranium helps distribute<br />
applied stresses efficiently over a large area<br />
<strong>and</strong> decreases stresses in the anterior <strong>cranial</strong><br />
<strong>base</strong> during loading of the temporom<strong>and</strong>ibular<br />
joint. This interesting model, however,<br />
requires further testing.<br />
Whether the spheroid shape of the telencephalon<br />
is a <strong>function</strong>al adaptation or a<br />
structural consequence of geometry <strong>and</strong><br />
developmental processes remains to be determined.<br />
Nevertheless, the presence of<br />
the cerebellum, <strong>and</strong> ultimately of the<br />
brain stem, prevents caudal expansion of<br />
the telencephalon, making rostral expansion<br />
of the telencephalon the easiest route.<br />
This would cause the especially large human<br />
brain to develop a kink of the kind<br />
measured by Hofer, which in turn may<br />
cause flexion of the basicranium. If this<br />
hypothesis is correct, then some proportion<br />
of the variation in basi<strong>cranial</strong> angle<br />
among <strong>primate</strong>s is caused by intrinsic<br />
changes in brain shape, <strong>and</strong> not the relationship<br />
between the size of the brain <strong>and</strong><br />
the <strong>base</strong> on which it sits.<br />
One caution (noted above) is that ontogenetic<br />
data suggest that the interspecific<br />
variation in <strong>cranial</strong> <strong>base</strong> angle <strong>and</strong> shape<br />
presented above is partially a consequence<br />
of variables other than relative encephalization<br />
or intrinsic brain shape. Ontogenetic<br />
data are useful because they allow one to<br />
examine temporal relationships among predicted<br />
causal factors. <strong>The</strong> human ontogenetic<br />
data provide mixed support for the<br />
hypothesis that <strong>cranial</strong> <strong>base</strong> angulation reflects<br />
relative encephalization. Jeffery<br />
(1999) found no significant relationship between<br />
CBA1 <strong>and</strong> IRE1 during the second<br />
fetal trimester in humans, when brain<br />
growth is especially rapid; but Lieberman<br />
<strong>and</strong> McCarthy (1999) found that the human<br />
<strong>cranial</strong> <strong>base</strong> flexes rapidly during the first 2<br />
postnatal years, when most brain growth<br />
occurs. Why relative brain size in humans<br />
correlates with <strong>cranial</strong> <strong>base</strong> angle after<br />
birth but not before remains to be explained.<br />
In addition, <strong>and</strong> in contrast to humans,<br />
the <strong>cranial</strong> <strong>base</strong> in all nonhuman <strong>primate</strong>s<br />
so far analyzed extends rather than<br />
flexes during the period of postnatal brain<br />
growth, <strong>and</strong> continues to extend throughout<br />
the period of facial growth, after brain<br />
growth has ceased. In Pan, for example, approximately<br />
88% of <strong>cranial</strong> <strong>base</strong> extension<br />
(CBA1) occurs after the brain has reached<br />
95% adult size (Lieberman <strong>and</strong> McCarthy,<br />
1999). Similar results characterize other<br />
genera (e.g., Macaca; Sirianni <strong>and</strong> Swindler,<br />
1985; Schneiderman, 1992).<br />
Ontogenetic data do not disprove the hypothesis<br />
that variation in <strong>cranial</strong> <strong>base</strong> angle<br />
is related to brain size, but instead highlight<br />
the likelihood that the processes which generate<br />
variation in <strong>cranial</strong> <strong>base</strong> angle are<br />
polyphasic <strong>and</strong> multifactorial. Notably, the<br />
ontogenetic data suggest that the tight<br />
structural relationship between the face<br />
<strong>and</strong> the anterior <strong>cranial</strong> <strong>base</strong> (discussed below)<br />
is also an important influence on <strong>cranial</strong><br />
<strong>base</strong> angle. This suggests that a large<br />
proportion of the interspecific variation in<br />
CBA, IRE, <strong>and</strong> other aspects of neural size<br />
<strong>and</strong> shape reported above is explained by<br />
interactions between the brain <strong>and</strong> the <strong>cranial</strong><br />
<strong>base</strong> prior to the end of the neural<br />
growth phase. <strong>The</strong>reafter, other factors (especially<br />
those related to the face) influence<br />
the shape of the <strong>cranial</strong> <strong>base</strong>. One obvious<br />
way to test this hypothesis is to compare the
138 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
above interspecific analyses of adults with<br />
comparable analyses of infants at the period<br />
when the brain has ceased growing, but before<br />
much of the face has grown.<br />
Brain volume <strong>and</strong> posterior <strong>cranial</strong><br />
fossa shape<br />
Dean <strong>and</strong> Wood (1981, 1982) <strong>and</strong> Aiello<br />
<strong>and</strong> Dean (1990) hypothesized that increases<br />
in cerebellum size correlate with increases<br />
in the size of the posterior <strong>cranial</strong><br />
fossa. This correlation is purportedly a result<br />
of increases in basi<strong>cranial</strong> flexion; <strong>and</strong><br />
by lateral <strong>and</strong> anterior displacement of the<br />
lateral aspects of the petrous pyramids,<br />
which cause the petrous pyramids to be<br />
more coronally oriented in humans than in<br />
great apes. However, Ross <strong>and</strong> Ravosa<br />
(1993) found little support for a link between<br />
absolute cerebellum volume <strong>and</strong><br />
CBA4; in addition, Spoor (1997) did not find<br />
a correlation between cerebellum volume<br />
<strong>and</strong> petrous orientation. Rather, Spoor<br />
(1997) showed that more coronally oriented<br />
petrous pyramids in adult <strong>primate</strong>s correlate<br />
better with increases in brain volume<br />
relative to basi<strong>cranial</strong> length. In addition,<br />
the petrous pyramids, when viewed from<br />
the internal aspect of the <strong>cranial</strong> <strong>base</strong>, are<br />
not more coronally oriented in humans vs.<br />
other apes (Spoor, 1997).<br />
<strong>The</strong> probable explanation for these results<br />
may be that the posterior <strong>cranial</strong> <strong>base</strong><br />
(Ba-S) scales with isometry against both<br />
cerebellum volume <strong>and</strong> the volume of infratentorial<br />
neural structures (cerebellum, medulla<br />
oblongata, mesencephalon) (Table 4).<br />
If this scaling pattern characterizes those<br />
dimensions of the posterior <strong>cranial</strong> fossa not<br />
in the mid-sagittal plane, then increased<br />
infratentorial neural volumes would not necessitate<br />
changes in the proportions of the<br />
entire posterior <strong>cranial</strong> fossa. This would<br />
imply that variation in the orientation of<br />
the petrous pyramids may be linked to<br />
changes in other <strong>cranial</strong> systems <strong>and</strong> is not<br />
solely a structural response to changes in<br />
cerebellar volume.<br />
ASSOCIATIONS BETWEEN CRANIAL<br />
BASE AND FACE<br />
It has long been known that the <strong>cranial</strong><br />
<strong>base</strong> plays an important role in facial<br />
growth, but many details of how these regions<br />
interact remain poorly understood.<br />
While the face has some influence on <strong>cranial</strong><br />
<strong>base</strong> growth (see below), there are two major<br />
reasons to believe that the <strong>cranial</strong> <strong>base</strong><br />
exerts a greater influence on the face than<br />
vice versa during growth by setting up certain<br />
key spatial relationships. First, the majority<br />
of the <strong>cranial</strong> <strong>base</strong> (with the exception<br />
of the ethmoidal portions of the ethmomaxillary<br />
complex) attains adult size long before<br />
the face (Moore <strong>and</strong> Lavelle, 1974). Second,<br />
as noted above, most of the face grows anteriorly,<br />
laterally, inferiorly, <strong>and</strong> around the<br />
<strong>cranial</strong> <strong>base</strong>. In all mammals, the upper<br />
portion of the face (the orbital <strong>and</strong> upper<br />
nasal regions) grows antero inferiorly relative<br />
to the anterior <strong>cranial</strong> <strong>base</strong> <strong>and</strong> floor;<br />
<strong>and</strong> the middle face (mostly the nasal region)<br />
grows anteriorly relative to the middle<br />
<strong>cranial</strong> fossa. <strong>The</strong> lower portion of the face<br />
(the m<strong>and</strong>ibular <strong>and</strong> maxillary arches <strong>and</strong><br />
their supporting structures) interacts only<br />
indirectly with the <strong>cranial</strong> <strong>base</strong>, since the<br />
maxillary arch grows inferiorly from the<br />
middle face <strong>and</strong> anteriorly relative to the<br />
pterygoid processes of the sphenoid.<br />
<strong>The</strong>se spatial <strong>and</strong> developmental associations<br />
raise an important question: to what<br />
extent does the <strong>cranial</strong> <strong>base</strong> influence facial<br />
growth <strong>and</strong> form? In order to address this<br />
issue, we first discuss the relationships between<br />
two regions of the face <strong>and</strong> <strong>cranial</strong><br />
<strong>base</strong> that are contiguous across <strong>function</strong>al<br />
or developmental boundaries (the so-called<br />
growth counterparts of Enlow, 1990): 1) the<br />
anterior <strong>cranial</strong> fossa <strong>and</strong> the upper, orbital,<br />
<strong>and</strong> nasal portions of the face, <strong>and</strong> 2) the<br />
middle <strong>cranial</strong> fossa <strong>and</strong> the middle, ethmomaxillary<br />
portion of the face. We conclude<br />
with a brief discussion of the possible relationships<br />
between <strong>cranial</strong> <strong>base</strong> shape <strong>and</strong><br />
overall facial shape.<br />
Anterior <strong>cranial</strong> fossa shape <strong>and</strong> upper<br />
facial growth<br />
<strong>The</strong> upper face comprises the orbital cavities,<br />
the orbital superstructures, <strong>and</strong> the<br />
upper portion of the nasal cavity. <strong>The</strong> upper<br />
face therefore incorporates elements of the<br />
anterior <strong>cranial</strong> <strong>base</strong>, including the ethmoid,<br />
parts of the sphenoid, <strong>and</strong> significant<br />
portions of the frontal bone. <strong>The</strong> upper face
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 139<br />
grows away from the rest of the <strong>cranial</strong> <strong>base</strong><br />
in three ways. Initially, as the eyeballs exp<strong>and</strong>,<br />
the orbital cavity exp<strong>and</strong>s anteriorly,<br />
inferiorly, <strong>and</strong> laterally through drift <strong>and</strong><br />
displacement (Moss <strong>and</strong> Young, 1960; Enlow,<br />
1990). Animals enucleated during the<br />
period of eyeball growth consequently have<br />
deficient anterior <strong>and</strong> lateral growth of the<br />
upper face (see Sarnat, 1982). In addition,<br />
since the roof of the orbit also contributes to<br />
the floor of the anterior <strong>cranial</strong> fossa (i.e.,<br />
the orbital plates of the frontal bone <strong>and</strong><br />
lesser wings of the sphenoid), the position,<br />
orientation, <strong>and</strong> shape of the orbital roof<br />
must inevitably be affected by growth of the<br />
frontal lobes <strong>and</strong> anterior <strong>cranial</strong> fossa. Finally,<br />
the orbital cavities <strong>and</strong> superstructures<br />
grow anteriorly <strong>and</strong> laterally away<br />
from the anterior <strong>cranial</strong> fossa, but only after<br />
some period of postnatal development.<br />
In humans, for example, the upper face does<br />
not emerge from under the anterior <strong>cranial</strong><br />
<strong>base</strong> until after the eruption of the second<br />
molars (Riolo et al., 1974; Lieberman, 2000).<br />
In contrast, the front of the upper face in<br />
most nonhuman <strong>primate</strong>s projects anteriorly<br />
relative to the front of the anterior <strong>cranial</strong><br />
fossa prior to the eruption of the first<br />
molars (Krogman, 1969; Lieberman, 1998,<br />
2000). Variation in this spatial separation,<br />
termed neuro<strong>cranial</strong>-orbital or neuro-orbital<br />
disjunction, has been analyzed by various<br />
researchers to explain ontogenetic <strong>and</strong><br />
interspecific patterns of supraorbital torus<br />
morphology (Weidenreich, 1941; Moss <strong>and</strong><br />
Young, 1960; Radinsky, 1968, 1970, 1977,<br />
1979; Shea, 1985a, 1986, 1988; Ravosa,<br />
1988, 1991a,b; Hyl<strong>and</strong>er <strong>and</strong> Ravosa, 1992;<br />
Vinyard <strong>and</strong> Smith, 1997; Lieberman, 1998,<br />
2000; Ravosa et al., 2000b).<br />
<strong>The</strong>se developmental <strong>and</strong> architectural<br />
relationships between the anterior <strong>cranial</strong><br />
<strong>base</strong> <strong>and</strong> upper face have several consequences<br />
for interspecific variation in <strong>primate</strong>s.<br />
First, the orientation of the orbits<br />
<strong>and</strong> the upper face is intimately related to<br />
the orientation of the anterior <strong>cranial</strong> <strong>base</strong><br />
in haplorhines (Ravosa, 1991a,b; Ross <strong>and</strong><br />
Ravosa, 1993; Ross <strong>and</strong> Henneberg, 1995),<br />
confirming the hypothesis of Dabelow (1929,<br />
1931) that the orientation of the orbits <strong>and</strong><br />
the anterior <strong>cranial</strong> <strong>base</strong> should be tightly<br />
correlated in animals like haplorhines,<br />
whose orbits are closely approximated below<br />
the olfactory tract (see also Cartmill,<br />
1970, 1972; Ravosa et al., 2000a,2000b).<br />
Several recent studies have found support<br />
for this hypothesis. First, brow-ridge size in<br />
anthropoids (but not strepsirhines) is highly<br />
correlated with variation in the position of<br />
the orbits relative to the anterior <strong>cranial</strong><br />
<strong>base</strong> (Ravosa, 1988, 1991a,b; Hyl<strong>and</strong>er <strong>and</strong><br />
Ravosa, 1992; Vinyard <strong>and</strong> Smith, 1997;<br />
Lieberman, 2000; Ravosa et al., 2000b). Finally,<br />
there is evidence that the upper face<br />
tends to be rotated dorsally relative to the<br />
posterior <strong>cranial</strong> <strong>base</strong> in <strong>primate</strong>s with a<br />
highly extended <strong>cranial</strong> <strong>base</strong>, but more ventrally<br />
rotated relative to the posterior <strong>cranial</strong><br />
<strong>base</strong> in <strong>primate</strong>s such as humans <strong>and</strong><br />
bonobos with a more flexed <strong>cranial</strong> <strong>base</strong> (Delattre<br />
<strong>and</strong> Fenart, 1956; Moss <strong>and</strong> Young,<br />
1960; Heintz, 1966; Cramer, 1977; Shea,<br />
1985a, 1986, 1988; Ravosa, 1988, 1991a,b;<br />
Lieberman, 2000).<br />
While the structural boundaries shared<br />
by the anterior <strong>cranial</strong> <strong>base</strong> <strong>and</strong> the upper<br />
face result in a high degree of integration<br />
between these two regions, the extent to<br />
which anterior <strong>cranial</strong> <strong>base</strong> shape influences<br />
other aspects of facial shape is less<br />
clear. In an interspecific study of 68 species,<br />
Ross <strong>and</strong> Ravosa (1993) found that both orbit<br />
<strong>and</strong> palate orientation are significantly<br />
correlated with anterior <strong>cranial</strong> <strong>base</strong> orientation,<br />
but that palate orientation accounts<br />
for none of the variation in <strong>cranial</strong> <strong>base</strong><br />
angle independent of orbital axis orientation.<br />
McCarthy <strong>and</strong> Lieberman (2001) have<br />
also shown that the orientation of the orbits<br />
<strong>and</strong> the anterior <strong>cranial</strong> <strong>base</strong> are correlated<br />
with each other (r 0.617, P 0.05) in<br />
haplorhines but not in strepsirhines. <strong>The</strong>se<br />
studies suggest that the orientation of the<br />
anterior <strong>cranial</strong> <strong>base</strong> affects the orientation<br />
of the upper face directly, but that it only<br />
indirectly influences palate orientation<br />
through the integration of palate <strong>and</strong> orbits<br />
(see also Ravosa, 1988; Ravosa <strong>and</strong> Shea,<br />
1994). Consequently, it seems likely that<br />
the anterior <strong>cranial</strong> <strong>base</strong> exerts a slight influence<br />
on facial orientation as a whole, but<br />
that only the orbital region of the face is<br />
directly integrated with the anterior <strong>cranial</strong><br />
<strong>base</strong>. Higher levels of integration appear to<br />
characterize those organisms with greater
140 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
TABLE 6. Descriptive statistics for orientation of the palate relative to the anterior <strong>cranial</strong> <strong>base</strong> in <strong>primate</strong>s,<br />
haplorhini, <strong>and</strong> strepsirrhini 1<br />
Planum sphenoideum<br />
Line from Sella to foramen caecum<br />
N Mean SD Minimum Maximum N Mean SD Minimum Maximum<br />
Primates 63 15.1 15.66 41.5 45.2 60 20.0 15.15 22.1 67.3<br />
Haplorhines 47 12.80 16.35 41.5 45.2 46 15.1 12.14 22.1 52.0<br />
Strepsirrhines 16 21.8 11.37 1.7 42.3 14 36.1 12.84 19.8 67.3<br />
1 Calculated from data in Ross <strong>and</strong> Ravosa (1993) <strong>and</strong> Ross <strong>and</strong> Henneberg (1995), <strong>and</strong> presented above by subtracting AFK from<br />
CBA4 <strong>and</strong> CBA1.<br />
encephalization, increased orbital convergence,<br />
<strong>and</strong> relatively large orbits (Ravosa et<br />
al., 2000a).<br />
Enlow (1990) proposed several structural<br />
relationships between the anterior <strong>cranial</strong><br />
<strong>base</strong> <strong>and</strong> various aspects of facial shape. His<br />
general model for the plan of the face is<br />
<strong>base</strong>d almost exclusively on analyses of human<br />
radiographs, <strong>and</strong> has not been carefully<br />
tested in most respects. However,<br />
three hypotheses are of special interest.<br />
First, since the floor of the nasal chamber is<br />
also the roof of the oral cavity, Enlow (1990)<br />
proposed that interorbital breadth should<br />
be correlated with prognathism because<br />
“the broad nasal <strong>base</strong> of most other mammals<br />
supports a correspondingly much<br />
longer snout.” Smith <strong>and</strong> Josell (1984)<br />
tested this hypothesis using a sample of 32<br />
<strong>primate</strong>s, <strong>and</strong> found a low correlation (r <br />
0.46) between interorbital breadth <strong>and</strong><br />
m<strong>and</strong>ibular prognathism, <strong>and</strong> noted that<br />
the correlation was even weaker when effects<br />
of overall <strong>cranial</strong> length <strong>and</strong> body size<br />
were taken into account. This is perhaps not<br />
surprising, as there is no obvious biomechanical<br />
or developmental reason why the<br />
length of the face should be correlated with<br />
the width of the posterior part of the face.<br />
Second, Enlow (1990) proposed that the orientation<br />
of the cribriform plate in all mammals,<br />
including <strong>primate</strong>s, is perpendicular<br />
to the orientation of the nasomaxillary complex<br />
(defined as a plane from the most anterior<br />
point on the frontal squama to the<br />
prosthion). Ravosa <strong>and</strong> Shea (1994) investigated<br />
the angle between the cribriform<br />
plane (measured in two ways) <strong>and</strong> the orientation<br />
of the midface (measured from the<br />
prosthion tangent to the endo<strong>cranial</strong> contour<br />
of the frontal) in a sample of Old World<br />
monkeys. <strong>The</strong>y found that when the cribriform<br />
plane was defined as the line connecting<br />
the anterior-most <strong>and</strong> posterior-most aspects<br />
of the cribriform plate, the mean angle<br />
between these planes was 93° for cercopithecines<br />
<strong>and</strong> 86° for colobines <strong>and</strong> was<br />
independent of face size. However, variability<br />
in this angle was relatively high; <strong>and</strong><br />
when the cribriform angle was measured as<br />
the line connecting the anterior-most <strong>and</strong><br />
posterior-most aspects of the cribriform<br />
plate at the ethmoid/nasal cavity junction,<br />
the angle was significantly different from<br />
90° <strong>and</strong> correlated with skull size. Thus,<br />
there is only limited support for the hypothesis<br />
that the cribriform plate <strong>and</strong> the orientation<br />
of the snout are perpendicular. Finally,<br />
Enlow (1990) <strong>and</strong> several others (e.g.,<br />
Sirianni <strong>and</strong> Swindler, 1979) have suggested<br />
that the palatal plane <strong>and</strong> the anterior<br />
<strong>cranial</strong> <strong>base</strong> (S-FC) should be roughly<br />
parallel across <strong>primate</strong>s when the cribriform<br />
plate is parallel to the planum sphenoideum.<br />
However, interspecific analysis of<br />
the orientation of the palate relative to both<br />
the planum sphenoideum <strong>and</strong> a line from<br />
the sella to the foramen caecum (Table 6)<br />
provide little support for the hypothesis of<br />
Enlow (1990) across Primates, Haplorhini,<br />
<strong>and</strong> Strepsirhini.<br />
Middle <strong>cranial</strong> fossa shape <strong>and</strong><br />
midfacial growth<br />
<strong>The</strong> second major region of interaction between<br />
the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> the face is along<br />
the junction between the middle <strong>cranial</strong><br />
fossa <strong>and</strong> the posterior margins of the midface.<br />
Whereas the upper face <strong>and</strong> anterior<br />
<strong>cranial</strong> fossa are tightly integrated because<br />
they share many of the same bony walls, the<br />
middle portion of the face (the ethmomaxillary<br />
complex) <strong>and</strong> middle <strong>cranial</strong> fossa are<br />
growth counterparts that may interact<br />
along their complex boundary, which lies<br />
more or less in the coronal plane (Hoyte,
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 141<br />
Fig. 10. Posterior maxillary (PM) plane <strong>and</strong> 90° orientation relative to the neutral horizontal axis<br />
(NHA) of the orbits; illustrated here in, Homo sapiens. <strong>The</strong> inferior <strong>and</strong> superior termini of the PM plane<br />
are, respectively, pterygomaxillary (Ptm) <strong>and</strong> the PM point (PMp). <strong>The</strong> anterior <strong>and</strong> posterior termini of<br />
the NHA are, respectively, OM <strong>and</strong> OA (see text for definitions).<br />
1991). In particular, the ethmomaxillary<br />
complex grows anteriorly, laterally, <strong>and</strong> inferiorly<br />
away from the middle <strong>cranial</strong> fossa<br />
at a number of primary growth sites (e.g.,<br />
the spheno-palatine suture, the spheno-zygomatic<br />
suture, <strong>and</strong> the spheno-ethmoid<br />
synchondrosis). Consequently, the shape of<br />
the middle <strong>cranial</strong> fossa, especially the<br />
greater wings of the sphenoid (which house<br />
the temporal lobes), must also play some<br />
role in influencing the orientation of the<br />
posterior margin of the ethmomaxillary<br />
complex <strong>and</strong> its position relative to the rest<br />
of the <strong>cranial</strong> <strong>base</strong>.<br />
Recent research on the integration of the<br />
middle <strong>cranial</strong> fossa <strong>and</strong> the midface has<br />
focused on the role of the posterior maxillary<br />
(PM) plane. <strong>The</strong> PM plane has been<br />
defined in several different ways (Enlow<br />
<strong>and</strong> Azuma, 1975; Enlow, 1976, 1990; Enlow<br />
<strong>and</strong> Hans, 1996), but we use here the<br />
definition of Enlow <strong>and</strong> Azuma (1975), as<br />
the line connecting two termini: 1) pterygomaxillary<br />
(Ptm), the average midline point<br />
of the most inferior <strong>and</strong> posterior points on<br />
the maxillary tuberosities; <strong>and</strong> 2) the PM<br />
point (PMp), the average midline point of<br />
the anterior-most points on the lamina of<br />
the greater wings of the sphenoid (for details,<br />
see McCarthy <strong>and</strong> Lieberman, 2001).<br />
<strong>The</strong>se points <strong>and</strong> their relationship to the<br />
<strong>cranial</strong> <strong>base</strong> <strong>and</strong> face are illustrated in Figure<br />
10. Note that because the PM plane is<br />
defined using two paired registration<br />
points, it is technically not a plane, but is<br />
instead an abstract line whose termini do<br />
not lie in the same parasagittal plane. Despite<br />
its abstract nature, the PM plane is a
142 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
potentially useful analytical concept for researchers<br />
interested in integration between<br />
the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> face because it effectively<br />
characterizes both the posterior margin<br />
of the face <strong>and</strong> the boundary between<br />
the anterior <strong>and</strong> middle <strong>cranial</strong> fossae in<br />
lateral radiographs. <strong>The</strong> inferior terminus,<br />
Ptm, is the posterolateral corner of the ethmomaxillary<br />
complex <strong>and</strong> lies just in front<br />
of the spheno-palatine suture (Williams et<br />
al., 1995). <strong>The</strong> superior terminus, PMp, is<br />
the anterior-most point of the middle <strong>cranial</strong><br />
fossa, lying close to the midpoint of the<br />
spheno-ethmoid synchondrosis <strong>and</strong> the midpoint<br />
of the spheno-frontal suture on the<br />
floor of the <strong>cranial</strong> <strong>base</strong> in all <strong>primate</strong>s (Van<br />
der Linden <strong>and</strong> Enlow, 1971; McCarthy,<br />
2001; McCarthy <strong>and</strong> Lieberman, 2001).<br />
Perhaps the most interesting aspect of the<br />
PM plane is its relationship to the orbits<br />
<strong>and</strong> the anterior <strong>cranial</strong> <strong>base</strong>. Several researchers<br />
have claimed that the PM plane<br />
always forms a 90° angle to the neutral horizontal<br />
axis (NHA) of the orbits (see Measurement<br />
Definitions). In their initial study,<br />
Enlow <strong>and</strong> Azuma (1975) found the PM-<br />
NHA angle to average 90° in a combined<br />
mammalian sample of 45 species, <strong>and</strong> 90° in<br />
a large sample of adult humans. Ravosa<br />
(1991a,b), <strong>and</strong> Ravosa <strong>and</strong> Shea (1994)<br />
tested the PM-NHA angle in a cross-sectional<br />
sample of macaques <strong>and</strong> two interspecific<br />
sample of adult <strong>primate</strong>s, <strong>and</strong> obtained<br />
consistent, but different PM-NHA<br />
angles from those of Enlow <strong>and</strong> Azuma<br />
(1975), that ranged between 18° <strong>and</strong> 5° below<br />
90°. However, these studies measured<br />
the PM plane <strong>and</strong> the NHA (the latter only<br />
slightly) differently, <strong>and</strong> several more recent<br />
studies have corroborated the original<br />
hypothesis of Enlow <strong>and</strong> Azuma (1975). In<br />
particular, Bromage (1992) found the PM-<br />
NHA angle in a cross-sectional sample of 45<br />
Pan troglodytes crania to be 89.2 3.4° SD<br />
for dental stage I, 90.5 3.1° SD for dental<br />
stage II, <strong>and</strong> 88.2 4.0° SD for dental stage<br />
III. However, these data show some significant<br />
variation during growth, <strong>and</strong> some<br />
adult crania have PM-NHA angles somewhat<br />
different from 90°, especially those for<br />
certain hominids. Lieberman (1998) found<br />
the PM-NHA angle to be 89.9 1.7° SD in a<br />
longitudinal series of humans (Denver<br />
Fig. 11. Histograms comparing mean PM-NHA angle<br />
in samples of 18 adult anthropoid species (top) <strong>and</strong><br />
15 adult strepsirrhines species (bottom). PM-NHA° is<br />
not significantly different from 90° in any species.<br />
Growth Study; n 353) aged 1 month<br />
through 17 years, 9 months. Also, McCarthy<br />
<strong>and</strong> Lieberman (in press) recently found the<br />
PM-NHA angle to average 90.0 0.38° SD<br />
in a pooled sample of adults from 18 anthropoid<br />
species, <strong>and</strong> 89.4 0.46° SD in a pooled<br />
sample of adults from 15 strepsirhine species<br />
(Fig. 11). Consequently, the PM-NHA<br />
does appear to be invariant in <strong>primate</strong>s,<br />
with values for the most part near 90°. It<br />
should be stressed, however, that the developmental<br />
<strong>and</strong> <strong>function</strong>al <strong>base</strong>s (if any) for<br />
this purported invariance are still unknown<br />
<strong>and</strong> require further study.<br />
<strong>The</strong> 90° PM-NHA angle is useful for examining<br />
craniofacial integration <strong>and</strong> variation<br />
because, as noted above, the NHA is<br />
tightly linked to the orientation of the anterior<br />
<strong>cranial</strong> fossa <strong>and</strong> the ethmomaxillary<br />
complex. <strong>The</strong> roofs of the orbits (which help
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 143<br />
define the NHA) comprise much of the floor<br />
of the anterior <strong>cranial</strong> fossa. <strong>The</strong>refore, it<br />
follows that the PM plane <strong>and</strong> the anterior<br />
<strong>cranial</strong> <strong>base</strong> should also form an approximately<br />
90° angle in <strong>primate</strong>s whose orbits<br />
are approximated to the midline. This hypothesis<br />
was tested by McCarthy <strong>and</strong><br />
Lieberman (2001), who found that the angle<br />
between the PM plane <strong>and</strong> the planum<br />
sphenoideum averaged 95.2 7.6° SD (n <br />
18) in anthropoids <strong>and</strong> 82.8 9.5° SD (n <br />
14) in strepsirhines. McCarthy <strong>and</strong> Lieberman<br />
(2001) also found that the angle between<br />
the PM plane <strong>and</strong> the midline anterior<br />
<strong>cranial</strong> <strong>base</strong> (from the sella to the<br />
foramen caecum) averages 89.2 9.97° SD<br />
(n 18) in anthropoids, but 70.6 10.5° SD<br />
(n 15) in strepsirrhines. <strong>The</strong> high st<strong>and</strong>ard<br />
deviations of these angles indicate that<br />
the integration between the back of the face<br />
<strong>and</strong> the anterior <strong>cranial</strong> <strong>base</strong> is not very<br />
strong. Ross <strong>and</strong> Ravosa (1993) also came to<br />
similar conclusions by comparing the orbital<br />
axis orientation relative to the posterior <strong>cranial</strong><br />
<strong>base</strong>, against the orientation of the planum<br />
sphenoideum relative to the posterior<br />
<strong>cranial</strong> <strong>base</strong>. <strong>The</strong> differences between anthropoids<br />
<strong>and</strong> strepsirhines in the relationship<br />
of the orbits to the <strong>cranial</strong> <strong>base</strong> can be<br />
explained by the fact that the roof of the<br />
orbits does not contribute to the midline<br />
<strong>cranial</strong> <strong>base</strong> in strepsirhines, <strong>and</strong> because<br />
the cribriform plate tends to be oriented<br />
more vertically relative to the planum sphenoideum<br />
in strepsirrhines than in anthropoids<br />
(Cartmill, 1970).<br />
<strong>The</strong> potential integration of the middle<br />
<strong>and</strong> anterior <strong>cranial</strong> fossae with the face (as<br />
measured via the PM plane) <strong>and</strong> the anterior<br />
<strong>cranial</strong> <strong>base</strong> raises several interesting<br />
issues. Most importantly, the top <strong>and</strong> back<br />
of the face appear to form an integrated<br />
unit, the “facial block” which rotates during<br />
<strong>ontogeny</strong> around an axis through the intersection<br />
of the anterior <strong>and</strong> middle <strong>cranial</strong><br />
fossae at the front of the greater wings of<br />
the sphenoid (McCarthy <strong>and</strong> Lieberman,<br />
2001). This facial block is characteristic of<br />
anthropoids but not strepsirhines, <strong>and</strong> manifests<br />
itself through correlations between<br />
<strong>cranial</strong> <strong>base</strong> angle <strong>and</strong> upper facial orientation<br />
in <strong>primate</strong>s (Weidenriech, 1941; Moss<br />
<strong>and</strong> Young, 1960; Biegert, 1963; Shea,<br />
1985a, 1986, 1988; Ravosa, 1988, 1991a,b;<br />
Ross <strong>and</strong> Ravosa, 1993; Ross, 1995a,b; May<br />
<strong>and</strong> Sheffer, 1999; Lieberman, 2000; Ravosa<br />
et al., 2000a, 2000b). In particular, as the<br />
anterior <strong>cranial</strong> <strong>base</strong> flexes relative to the<br />
posterior <strong>cranial</strong> <strong>base</strong>, the PM plane also<br />
must flex relative to the posterior <strong>cranial</strong><br />
<strong>base</strong>, rotating the posterior <strong>and</strong> upper portions<br />
of the face underneath the anterior<br />
<strong>cranial</strong> fossa (klinorhynchy). In contrast, extension<br />
of the anterior <strong>cranial</strong> <strong>base</strong> relative<br />
to the posterior <strong>cranial</strong> <strong>base</strong> will rotate the<br />
posterior <strong>and</strong> upper portions of the face dorsally<br />
relative to the posterior <strong>cranial</strong> <strong>base</strong><br />
(airorhynchy) (Fig. 12).<br />
<strong>The</strong> relationship of the orientation of the<br />
back of the face (as measured for example by<br />
the PM plane) to the anterior <strong>cranial</strong> <strong>base</strong><br />
also influences nasopharynx shape. As Figure<br />
12 shows, flexion of the anterior <strong>cranial</strong><br />
<strong>base</strong> <strong>and</strong>/or face relative to the posterior<br />
<strong>cranial</strong> <strong>base</strong> not only rotates the face under<br />
the anterior <strong>cranial</strong> fossa, but it also shortens<br />
(absolutely <strong>and</strong> relatively) the length of<br />
the pharyngeal space between the back of<br />
the palate <strong>and</strong> the front of the vertebral<br />
column (Laitman <strong>and</strong> Heimbuch, 1982;<br />
Spoor et al., 1999; McCarthy <strong>and</strong> Lieberman,<br />
2001). While flexion of the <strong>cranial</strong> <strong>base</strong><br />
during <strong>ontogeny</strong> is completely independent<br />
of the descent of the hyoid <strong>and</strong> larynx<br />
(Lieberman <strong>and</strong> McCarthy, 1999), variation<br />
in <strong>cranial</strong> <strong>base</strong> angle does influence some<br />
aspects of pharyngeal shape (Laitman <strong>and</strong><br />
Heimbuch, 1982; see below).<br />
Ross <strong>and</strong> Henneberg (1995) suggested<br />
that there must be <strong>function</strong>al constraints on<br />
how far back the hard palate can be positioned<br />
without occluding the airway. <strong>The</strong><br />
integration of the anterior <strong>cranial</strong> <strong>base</strong> with<br />
the upper <strong>and</strong> posterior margins of the face<br />
means that these constraints on pharynx<br />
position might determine the maximum<br />
possible degree of basi<strong>cranial</strong> angle, particularly<br />
in genera such as Pongo <strong>and</strong> Alouatta<br />
with relatively large pharyngeal structures<br />
(Biegert, 1957, 1963). Ross <strong>and</strong> Henneberg<br />
(1995) suggested that hominoids might<br />
have found a way to circumvent these “constraints.”<br />
Hominoids have more airorhynch<br />
(dorsally rotated <strong>and</strong> less frontated) orbits<br />
<strong>and</strong> palates than nonhominoid <strong>primate</strong>s<br />
with comparably flexed basicrania (Shea,
144 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Fig. 12. Proposed “facial block,” showing the effects of angular invariance between the back of the face<br />
(summarized by the PM plane) <strong>and</strong> the top of the face, which is also the bottom of the anterior <strong>cranial</strong><br />
<strong>base</strong> (S-FC). Changes in <strong>cranial</strong> <strong>base</strong> angle cause the top <strong>and</strong> back of the face to rotate together around<br />
an imaginary axis through the PM point. See text for details.<br />
1985a, 1988; Ross <strong>and</strong> Henneberg, 1995).<br />
This airorhynchy has yet to be explained<br />
developmentally <strong>and</strong> <strong>function</strong>ally; however,<br />
Ross <strong>and</strong> Henneberg (1995) suggested that<br />
it evolved in hominoids in response to increased<br />
flexion of the <strong>cranial</strong> <strong>base</strong> producing<br />
posterior displacement of the palate.<br />
More research is needed on the integration<br />
of the midface <strong>and</strong> <strong>cranial</strong> <strong>base</strong>. In particular,<br />
why is the PM plane oriented at 90°<br />
relative to the NHA during postnatal <strong>ontogeny</strong><br />
<strong>and</strong> thus across taxa? Another question<br />
of interest is, what aspects of <strong>cranial</strong> <strong>base</strong><br />
<strong>and</strong> facial shape are responsible for most of<br />
the variation in PM plane position, <strong>and</strong><br />
hence facial orientation? This problem has<br />
not been well studied, but the orientation of<br />
the PM plane is probably most affected by<br />
the size of the middle <strong>cranial</strong> fossa, especially<br />
the length of the temporal lobes, by<br />
flexion of the sphenoid, <strong>and</strong> by the length of<br />
the anterior sphenoid in the midline <strong>cranial</strong><br />
<strong>base</strong>. Three-dimensional studies of the interface<br />
between the PM plane <strong>and</strong> the <strong>cranial</strong><br />
<strong>base</strong> are needed to resolve these <strong>and</strong><br />
other questions about <strong>cranial</strong> <strong>base</strong>-face interrelations<br />
<strong>and</strong> interactions.<br />
Basi<strong>cranial</strong> width <strong>and</strong> overall facial<br />
shape in humans<br />
Although it is clear that the <strong>cranial</strong> <strong>base</strong><br />
plays a major role in influencing facial orientation<br />
relative to the neurocranium, there<br />
is less information about the potential influence<br />
of the <strong>cranial</strong> <strong>base</strong> on other aspects of<br />
facial shape such as height, length, <strong>and</strong><br />
width. To what extent is overall facial shape<br />
independent of the <strong>cranial</strong> <strong>base</strong>? It is commonly<br />
assumed that the majority of facial<br />
growth is independent of <strong>cranial</strong> <strong>base</strong><br />
growth, largely because much of the face<br />
grows in a skeletal growth trajectory after<br />
the end of the neural growth phase. In humans,<br />
for example, the face attains 95%<br />
adult size by 16–18 years, at least 10 years<br />
after the <strong>cranial</strong> <strong>base</strong> reaches adult size<br />
(Stamrud, 1959; Moore <strong>and</strong> Lavelle, 1974).<br />
In addition, most facial <strong>and</strong> basi<strong>cranial</strong> dimensions<br />
appear to be genetically independent<br />
in adults (Cheverud, 1996). However,<br />
there is some evidence to suggest that<br />
changes in the proportions of the <strong>cranial</strong><br />
<strong>base</strong> can influence facial shape. This interaction<br />
is predicted to be especially important,<br />
<strong>and</strong> perhaps exclusive to humans, in<br />
which the upper face lies almost completely<br />
underneath the anterior <strong>cranial</strong> fossa (Weidenreich,<br />
1941; Howells, 1973; Enlow <strong>and</strong><br />
Bhatt, 1984; Enlow, 1990; Lieberman et al.,<br />
2000).<br />
<strong>The</strong> most explicit of these hypotheses is<br />
that of Enlow (1990), who suggested that<br />
humans with absolutely narrow <strong>cranial</strong><br />
<strong>base</strong>s (primarily dolichocephalics) tend to
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 145<br />
Fig. 13. Diagram illustrating angles <strong>and</strong> lines used<br />
to calculate foramen magnum orientation relative to<br />
orbital axis orientation <strong>and</strong> head-neck angle (Strait <strong>and</strong><br />
Ross, 1999). <strong>The</strong> orientation of the orbital aperture <strong>and</strong><br />
the neck inclination were measured relative to gravity<br />
from videos (see Strait <strong>and</strong> Ross, 1999, for details). <strong>The</strong><br />
orientation of the foramen magnum relative to the orbital<br />
axis was calculated from measures of the orientation<br />
of both these planes relative to the clivus ossis<br />
occipitalis (CO) as 180°-AOA-FM CO.<br />
have longer, more flexed <strong>cranial</strong> <strong>base</strong>s, <strong>and</strong><br />
narrower faces than individuals with absolutely<br />
wider <strong>cranial</strong> <strong>base</strong>s (primarily<br />
brachycephalics). If variation in overall facial<br />
size is partially independent of <strong>cranial</strong><br />
<strong>base</strong> <strong>and</strong> neuro<strong>cranial</strong> size, then interactions<br />
between <strong>cranial</strong> <strong>base</strong> width <strong>and</strong> facial<br />
width may have some effects on facial<br />
height <strong>and</strong> length. Enlow (1990) proposed<br />
that humans with absolutely narrower <strong>cranial</strong><br />
<strong>base</strong>s tend to have proportionately narrower<br />
<strong>and</strong> antero-posteriorly longer faces<br />
(leptoproscopy) than humans with wider<br />
<strong>cranial</strong> <strong>base</strong>s, who tend to have proportionately<br />
wider <strong>and</strong> antero-posteriorly shorter<br />
faces (euryproscopy). <strong>The</strong> hypothesis receives<br />
some support from studies of artificial<br />
<strong>cranial</strong> deformation in humans. Antón<br />
(1989, 1994), for example, showed that antero-posterior<br />
head-binding during the first<br />
years of life causes not only a wider neurocranium<br />
but also a concomitantly wider face<br />
from additional growth in the most lateral<br />
regions; conversely, circumferential headbinding<br />
results in a narrower neurocranium<br />
<strong>and</strong> face. Lieberman et al. (2000) attempted<br />
to test the hypothesis of Enlow (1990) more<br />
directly with a partial correlation analysis<br />
of a sample of 98 adults from five geographically<br />
<strong>and</strong> craniometrically diverse populations.<br />
<strong>The</strong> study, however, found a low correlation<br />
between upper facial breadth <strong>and</strong><br />
maximum anterior <strong>cranial</strong> fossa breadth<br />
(r 0.53, P 0.001), <strong>and</strong> between midfacial<br />
breadth <strong>and</strong> maximum middle <strong>cranial</strong> fossa<br />
breadth (r 0.49; P 0.001) when differences<br />
in overall size were accounted for using<br />
partial correlation analysis. In addition,<br />
there was only a low tendency (r 0.49, P <br />
0.001) 5 for individuals with narrow <strong>cranial</strong><br />
<strong>base</strong>s to have longer, narrower faces than<br />
individuals with wider <strong>cranial</strong> <strong>base</strong>s, <strong>and</strong><br />
the trend may largely be a factor of interpopulation<br />
rather than intrapopulation<br />
variation. Further studies are needed to<br />
better underst<strong>and</strong> these sources of varia-<br />
5 r 0.40, P 0.001 when facial size is held constant (for<br />
details, see Lieberman et al., 2000).
TABLE 7. Mean values for measures of <strong>cranial</strong> <strong>base</strong> angulation, foramen magnum orientation, <strong>cranial</strong> <strong>base</strong> length, <strong>and</strong> measures of endo<strong>cranial</strong> volume,<br />
including data from Ross <strong>and</strong> Ravosa (1993), Ross <strong>and</strong> Henneberg (1995), <strong>and</strong> new data collected for this study<br />
Species or specimen IRE1 1 IRE5 2 (degrees)<br />
CBA4 1<br />
CBA1<br />
(degrees)<br />
AOA 1<br />
(degrees)<br />
AFK 1<br />
(degrees)<br />
Op-Ba clivus<br />
(degrees) 2<br />
Basion-sella<br />
(mm) 2<br />
Sella-foramen<br />
cecum (mm) 2<br />
Alouatta belzebul 0.680 0.062 186.0 183.3 192.670 175.170 116.170 23.223 36.344<br />
Alouatta palliata 0.710 0.065 188.0 180.7 190.170 174.830 23.509 34.252<br />
Aotus trivirgatus 0.901 0.082 180.0 176.8 168.500 147.830 126.500 11.250 21.014<br />
Arctocebus calabarensis 0.761 0.063 168.0 194.4 175.800 157.200 128.200 13.100 17.320<br />
Ateles fusciceps 0.916 0.085 162.0 170.3 169.500 156.660 118.830 22.593 33.015<br />
Avahi laniger 0.824 0.068 180.0 183.7 174.830 153.170 123.500 13.625 18.224<br />
Brachyteles arachnoides 0.883 0.083 161.0 172.5 170.400 159.400 126.500 24.024 34.352<br />
Cacajao calvus 0.860 0.087 172.0 168.2 173.000 158.830 122.000 19.757 27.689<br />
Callicebus moloch 0.775 0.074 176.0 176.0 164.000 156.400 131.800 15.320 19.631<br />
Callimico goeldi 0.817 0.078 171.0 165.0 154.670 141.500 133.200 11.175 18.425<br />
Callithrix argentata 0.771 0.074 164.0 164.8 152.000 144.330 123.830 10.443 16.929<br />
Cebuella pygmaea 0.880 0.071 171.0 164.2 153.000 141.500 115.330 8.454 13.906<br />
Cebus apella 0.868 0.082 173.0 166.6 165.830 154.170 123.000 20.794 27.890<br />
Cercocebus torquatus 0.874 0.083 172.0 157.3 161.400 142.000 130.000 21.734 33.663<br />
Cercopithecus aethiops 0.881 0.084 171.0 165.2 163.600 143.400 128.400 18.951 28.462<br />
Cercopithecus campbelli 0.879 0.079 170.0 161.2 160.330 142.170 126.670 16.460 32.825<br />
Cercopithecus mitis 0.832 0.080 179.0 170.0 166.170 142.830 128.830 20.226 31.501<br />
Cheirogaleus major 0.664 181.0 186.8 176.750 154.000 108.750 13.818<br />
Chiropotes satanas 0.850 0.085 170.0 169.5 169.830 157.833 128.000 18.543 26.481<br />
Daubentonia madgascariensis 0.930 157.0 169.2 169.600 147.600 110.600 19.762<br />
Erythrocebus patas 0.824 0.080 167.0 158.7 152.170 134.833 125.500 22.377 35.374<br />
Eulemur fulvus 0.768 0.064 171.0 183.7 177.000 158.000 126.170 19.351 25.150<br />
Euoticus elegantulus 0.827 0.065 158.0 177.7 160.500 140.830 120.500 8.989 18.417<br />
Gorilla gorilla 1.021 0.086 148.0 157.3 163.000 150.200 124.670 43.777 48.110<br />
Hapalemur griseus 0.795 0.064 175.0 179.5 173.170 144.170 110.600 13.809 23.179<br />
Homo sapiens 1.635 0.118 112.0 137.5 163.330 153.500 123.670 42.751 50.598<br />
Hylobates lar 0.918 0.084 153.0 168.3 165.500 158.333 129.334 22.265 32.856<br />
Hylobates moloch 0.943 0.085 160.0 172.5 175.670 159.330 117.000 21.749 30.632<br />
Indri indri 0.704 0.060 168.0 186.2 175.670 166.330 124.200 25.183 29.202<br />
Lagothrix lagotricha 0.879 0.082 176.0 176.0 162.330 151.400 123.400 24.909 31.039<br />
Leontopithecus rosalia 0.804 0.076 173.0 172.5 177.500 154.500 125.500 11.211 19.259<br />
Lepilemur mustelinus 0.811 178.0 181.2 158.330 143.170 128.170 12.149<br />
Lophocebus albigena 0.877 0.085 163.0 161.5 187.000 163.750 144.000 24.181 30.611<br />
Loris tardigradus 0.848 0.079 162.0 187.0 152.500 119.667 117.167 10.432 13.090<br />
Macaca nigra 0.880 0.081 158.0 151.0 154.000 134.500 122.250 22.108 32.258<br />
Macaca sylvana 0.865 0.083 154.0 159.2 150.000 23.086 32.901<br />
M<strong>and</strong>rillus leucopaeus 0.842 0.079 160.0 155.0 154.600 130.600 123.000 33.170 38.816<br />
M<strong>and</strong>rillus sphinx 0.828 0.080 154.0 152.5 154.583 116.750 27.404 39.082<br />
Microcebus murinus 0.820 157.0 157.830 142.833 128.000<br />
Miopithecus talapoin 0.955 0.096 168.0 164.2 180.000 150.000 105.000 13.612 22.387<br />
Mirza coquereli 0.666 0.057 158.0 189.0 156.670 138.167 121.167 11.991 18.179<br />
Nasalis larvatus 0.890 158.0 188.170 161.330 129.330<br />
Nycticebus coucang 0.747 0.065 171.0 185.5 166.830 146.330 118.670 12.933 21.012<br />
(Continued)
Species or specimen IRE1 1 IRE5 2 (degrees)<br />
CBA4 1<br />
TABLE 7. (Continued)<br />
CBA1<br />
(degrees)<br />
AOA 1<br />
(degrees)<br />
AFK 1<br />
(degrees)<br />
Op-Ba clivus<br />
(degrees) 2<br />
Basion-sella<br />
(mm) 2<br />
Sella-foramen<br />
cecum (mm) 2<br />
Otolemur crassicaudatus 0.753 0.060 167.0 178.7 160.670 155.830 132.670 14.908 23.434<br />
Pan troglodytes 1.039 0.091 152.0 158.7 151.670 123.000 121.830 35.633 45.114<br />
Papio anubis 0.865 0.084 154.0 153.2 196.830 175.330 124.000 29.010 36.697<br />
Perodicticus potto 0.731 181.0 157.500 146.333 122.834 17.820<br />
Piliocolobus badius 0.891 0.080 156.0 166.5 176.670 161.000 115.500 21.070 30.809<br />
Pithecia pithecia 0.771 0.074 182.0 175.8 167.400 162.000 116.000 17.670 25.883<br />
Pongo pygmaeus 1.026 0.085 135.0 160.8 147.000 138.830 115.000 41.228 44.834<br />
Semnopithecus entellus 0.906 0.081 148.0 159.8 150.830 145.330 122.830 21.870 33.094<br />
Presbytis melalophos 0.917 0.087 154.0 160.7 151.830 143.500 120.670 18.318 28.798<br />
Presbytis rubicunda 0.886 0.087 152.0 159.0 159.200 143.750 124.750 20.201 28.047<br />
Procolobus verus 0.874 0.081 157.0 171.4 166.830 154.500 121.670 18.631 28.264<br />
Propithecus verreauxi 0.788 0.068 168.0 184.8 148.570 137.000 117.714 20.548 25.056<br />
Pygathrix nemaeus 0.933 0.087 145.0 156.1 151.330 143.500 120.833 20.451 30.254<br />
Rhinopithecus roxellanae 1.002 0.089 150.0 157.2 154.500 143.830 121.340 21.601 32.294<br />
Saguinus fuscicollis 0.769 0.075 170.0 164.5 155.670 140.000 113.500 10.395 17.039<br />
Saimiri sciureus 0.926 0.087 169.0 165.5 153.170 135.330 118.000 12.046 20.672<br />
Simias concolor 0.786 0.079 161.0 160.2 174.670 160.833 129.167 19.658 28.526<br />
Symphalangus syndactylus 0.868 0.078 167.0 173.7 139.000 121.750 115.000 27.721 37.234<br />
Tarsius syrichta 1.005 0.062 141.0 151.0 149.000 133.000 119.833 6.099 14.796<br />
<strong>The</strong>ropithecus gelada 0.841 0.084 152.0 156.5 163.000 146.833 123.000 26.796 33.425<br />
Trachypithecus cristata 0.857 0.076 166.0 168.0 176.170 157.500 117.670 22.247 30.804<br />
Varecia variegata 0.752 0.062 177.0 187.8 21.726 29.495<br />
WT 17000 0.088 156.0<br />
OH5 0.098 135.0<br />
Sts 5 1.292 0.100 112.5 147.0 36.700 41.700<br />
1 Data primarily from Ross <strong>and</strong> Ravosa (1993).<br />
2 New data collected for this study from same radiographic collection as for Ross <strong>and</strong> Ravosa (1993).
148 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
tion, <strong>and</strong> also to study potential interactions<br />
between <strong>cranial</strong> <strong>base</strong> shape <strong>and</strong> facial shape<br />
in <strong>primate</strong>s <strong>and</strong> other mammals.<br />
THE CRANIAL BASE AND POSTURE<br />
Apart from a few recent studies reviewed<br />
here, little is known about the relationship<br />
between basi<strong>cranial</strong> morphology, head <strong>and</strong><br />
neck posture, <strong>and</strong> other aspects of head<br />
morphology related to locomotion. One persistent<br />
hypothesis that is especially relevant<br />
to hominin evolution is that flexion of<br />
the <strong>cranial</strong> <strong>base</strong> is an adaptation for orthograde<br />
posture in hominins because it causes<br />
the foramen magnum to have a relatively<br />
more anterior position <strong>and</strong> ventral orientation<br />
(Bolk, 1909, 1910; Duckworth, 1915;<br />
Weidenreich, 1941; Schultz, 1942, 1955;<br />
Ashton <strong>and</strong> Zuckerman, 1952, 1956; Ashton,<br />
1952; Moore et al., 1973; Adams <strong>and</strong><br />
Moore, 1975; DuBrul, 1977, 1979; Dean <strong>and</strong><br />
Wood, 1981, 1982). Indeed, these features<br />
are often invoked in attempts to reconstruct<br />
head posture in fossil hominins (e.g., White<br />
et al., 1994). All <strong>primate</strong>s have the center of<br />
mass of the head located anterior to the<br />
occipital condyles, such that more anteriorly<br />
positioned occipital condyles relative to<br />
head length reduce the lever arm between<br />
the center of mass <strong>and</strong> the atlanto-occipital<br />
joint. This balancing, in turn, reduces torque<br />
about this joint, thereby reducing the magnitude<br />
of the force required from the nuchal<br />
muscles to hold up the head (Schultz, 1942).<br />
<strong>The</strong> occipital condyles can be moved rostrally<br />
relative to overall head length by flexing<br />
the basicranium <strong>and</strong>/or shortening the<br />
posterior <strong>cranial</strong> <strong>base</strong>. In vitro experiments<br />
by Demes (1985) demonstrated that the<br />
more ventral orientation of rostrally placed<br />
occipital condyles orients the articular surfaces<br />
closer to perpendicular to the compressive<br />
force acting through the center of mass<br />
of the head, potentially reducing shearing<br />
forces acting across the joint that need to be<br />
resisted by muscles or ligaments.<br />
<strong>The</strong>re are some experimental data that<br />
rodents forced to walk bipedally (Moss,<br />
1961; Fenart, 1966; Riesenfeld, 1966) develop<br />
more flexed <strong>cranial</strong> <strong>base</strong>s. However,<br />
the hypothesis that variations in <strong>cranial</strong><br />
<strong>base</strong> angle are adaptations for head posture,<br />
however, is not well supported by comparative<br />
data. Among <strong>primate</strong>s, basi<strong>cranial</strong> flexion<br />
has been shown to be uncorrelated with<br />
either qualitative estimates of body posture<br />
(Ross <strong>and</strong> Ravosa, 1993) or quantitative<br />
measures of head <strong>and</strong> neck orientation<br />
(Strait <strong>and</strong> Ross, 1999). <strong>The</strong> partial correlation<br />
analysis of Strait <strong>and</strong> Ross (1999) confirmed<br />
relative brain size as a more important<br />
determinant of variation in basi<strong>cranial</strong><br />
angle, even when facial orientation <strong>and</strong><br />
head <strong>and</strong> neck posture were taken into account.<br />
Although foramen magnum orientation<br />
relative to anterior <strong>cranial</strong> <strong>base</strong> orientation<br />
(S-FC) has been shown to be related<br />
to relative brain size (Biegert, 1963; Spoor,<br />
1997), the relationship between head <strong>and</strong><br />
neck posture <strong>and</strong> foramen magnum orientation<br />
has not yet been evaluated.<br />
We gathered data on foramen magnum<br />
orientation (FM) from the same radiographs<br />
used by Ross <strong>and</strong> Ravosa (1993) <strong>and</strong> Ravosa<br />
(1991b), <strong>and</strong> combined these data with measures<br />
of hominids reported by Spoor (1993)<br />
<strong>and</strong> with measures of head <strong>and</strong> neck orientation<br />
reported by Strait <strong>and</strong> Ross (1999)<br />
(Fig. 13). <strong>The</strong> head-neck angle is the angle<br />
between neck inclination <strong>and</strong> orbit inclination,<br />
both relative to the substrate (Strait<br />
<strong>and</strong> Ross, 1999). <strong>The</strong> values for FM orientation<br />
relative to the clivus (FM CO) are in<br />
Table 7 <strong>and</strong> are summarized in Figure 14.<br />
<strong>The</strong> values for FM orientation relative to<br />
the orbital axis were calculated from measures<br />
of the orientation of both these planes<br />
relative to the clivus ossis occipitalis (CO) as<br />
180°-AOA-FM CO. <strong>The</strong>se data show that<br />
FM CO is not significantly correlated<br />
with basi<strong>cranial</strong> flexion, orbital axis orientation,<br />
the orientation of the head relative<br />
to the neck, or the size of the cerebellum<br />
relative to the posterior basicranium (Table<br />
8). Nor is foramen magnum orientation relative<br />
to the orbital axis (FM AOA) correlated<br />
with any of these variables, except<br />
AOA (Table 8). Of particular interest is the<br />
lack of correlation between the head-neck<br />
angle of Strait <strong>and</strong> Ross (1999) (Fig. 14),<br />
suggesting that foramen magnum orientation<br />
is not a good indicator of the orientation<br />
of the neck during habitual locomotion. This<br />
calls into question attempts to estimate<br />
head <strong>and</strong> neck posture from data on foramen<br />
magnum orientation in fossils.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 149<br />
Fig. 14. Bivariate plot of foramen magnum orientation relative to orbital axis (new data) against<br />
head-neck angle (Strait <strong>and</strong> Ross, 1999). Homo has unusually airorhynch (dorsally rotated) orbits<br />
relative to its foramen magnum orientation. Across <strong>primate</strong>s the relationship between these variables is<br />
significant (r 0.541, P 0.05); across nonhuman <strong>primate</strong>s r 0.691 (P 0.01).<br />
TABLE 8. Pearson’s r <strong>and</strong> P-values for correlations<br />
between measures of foramen magnum orientation <strong>and</strong><br />
measures of head morphology <strong>and</strong> orientation<br />
FM AOA FM CO<br />
r P r P<br />
CBA1 0.482 0.2 0.160 0.6<br />
CBA4 0.145 0.7 0.258 0.5<br />
AOA 0.841 0.001* 0.378 0.3<br />
Head-neck angle 0.405 0.2 0.202 0.6<br />
Cerebellum/B-a-se 0.169 0.6 0.170 0.6<br />
* P 0.05.<br />
Another widely accepted notion holds that<br />
a shift to orthogrady necessitates ventral<br />
flexion of the face, particularly the orbits,<br />
relative to the rest of the skull so that animals<br />
can continue to look rostrally (reviewed<br />
in Ross, 1995a; Strait <strong>and</strong> Ross,<br />
1999). Strait <strong>and</strong> Ross (1999) found that<br />
most <strong>primate</strong>s orient their orbits slightly<br />
downwards during locomotion. When other<br />
variables are controlled for using partial<br />
correlation analysis, orbital axis orientation<br />
relative to the posterior <strong>cranial</strong> <strong>base</strong> correlates<br />
significantly with head <strong>and</strong> neck posture.<br />
<strong>The</strong>se findings suggest that the direction<br />
of gaze cannot be reoriented through<br />
evolution solely by alterations in neck orientation<br />
or head orientation relative to the<br />
neck, <strong>and</strong> that there is a relationship between<br />
locomotor behavior <strong>and</strong> orbit orientation<br />
relative to the rest of the skull.<br />
This latter conclusion also explains why<br />
the orientation of the lateral semicircular<br />
canal (LSC) may correlate with head posture<br />
(Fenart <strong>and</strong> Pellerin, 1988 <strong>and</strong> references<br />
therein). Humans <strong>and</strong> animals of<br />
varying postures habitually hold their<br />
heads with the LSCs pitched upwards by<br />
several degrees (Sakka et al., 1976; Vidal et<br />
al., 1986; Graf et al., 1995). <strong>The</strong> semicircular<br />
canals <strong>function</strong> as accelerometers, registering<br />
changes in head velocity (or changes<br />
therein, i.e., acceleration), not head orientation<br />
relative to gravity (which is accomplished<br />
using the otolith organs). Thus, the<br />
intrinsic <strong>function</strong> of the canals does not explain<br />
any relationship between LSC orientation<br />
<strong>and</strong> head posture. An alternative,
150 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Fig. 15. Bivariate plot of orbital axis orientation relative to clivus (AOA) (Ross <strong>and</strong> Henneberg, 1995)<br />
against lateral semicircular canal (LSC) orientation relative to a line from basion to nasion (Spoor, 1993).<br />
<strong>The</strong> two variables are significantly correlated across all <strong>primate</strong>s (r 0.745, P 0.01) <strong>and</strong> nonhuman<br />
<strong>primate</strong>s (r 0.906, P 0.0001). Homo has unusually airorhynch (dorsally rotated) orbits for its LSC<br />
orientation (see also Ross <strong>and</strong> Henneberg, 1995; Strait <strong>and</strong> Ross, 1999).<br />
more likely answer lies in the role of the<br />
semicircular canals in vestibulo-ocular reflexes<br />
(VORs). VORs maintain a stable retinal<br />
image during head movements by coordinating<br />
eye movements with changes in<br />
head velocity. To achieve this, each semicircular<br />
canal is wired up to two extraocular<br />
muscles via a three-neuron reflex arc. 6 Because<br />
reflex arcs are evolutionarily conservative<br />
(Graf, 1988), each semicircular canal<br />
must remain roughly parallel with the line<br />
of action of the two extraocular muscles to<br />
which it provides primary excitatory input<br />
during VORs. This <strong>function</strong>al constraint<br />
predicts that evolutionary changes in medial<br />
<strong>and</strong> lateral rectus orientation will be<br />
associated with changes in LSC orientation.<br />
Because the medial <strong>and</strong> lateral recti arise<br />
6 Each posterior semicircular canal is connected to its ipsilateral<br />
superior oblique <strong>and</strong> contralateral inferior rectus, each anterior<br />
semicircular canal to its ipsilateral superior rectus <strong>and</strong> its<br />
contralateral inferior oblique, <strong>and</strong> each LSC to its ipsilateral<br />
medial rectus <strong>and</strong> contralateral lateral rectus (K<strong>and</strong>el et al.,<br />
1991).<br />
from the annulus tendineus around the optic<br />
canal <strong>and</strong> insert on the equator of the<br />
eyeball, they lie roughly in the same transverse<br />
plane as the orbital axis (see Measurement<br />
Definitions). Thus, LSC orientation<br />
should be correlated with orbital axis orientation.<br />
As an initial test of this hypothesis, Figure<br />
15 plots AOA (orbital axis orientation<br />
relative to CO) (data from Ross <strong>and</strong> Henneberg,<br />
1995) against LSC orientation relative<br />
to a line from basion to sella (ba-s)<br />
(Spoor <strong>and</strong> Zonneveld, 1998). Because CO is<br />
very similar to the line from ba-s in most<br />
taxa, these two angles roughly reflect the<br />
orientations of the LSC <strong>and</strong> the orbital axis<br />
both relative to the occipital clivus. Although<br />
these data derive from different<br />
specimens, a significant relationship is observed:<br />
LSC orientation is closely correlated<br />
with orbit orientation (r 0.824; the negative<br />
correlation reflects the fact that the<br />
LSC ba-s angle is measured above the<br />
LSC line, while the AOA angle is measured
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 151<br />
below the orbital axis line). <strong>The</strong>se data<br />
therefore lend support to the hypothesis<br />
that animals orient their heads at rest (<strong>and</strong><br />
during locomotion) primarily to orient their<br />
eyes towards the horizon rather than to orient<br />
their semicircular canals in any particular<br />
way. In sum, orbital axis orientation<br />
relative to the clivus <strong>and</strong> foramen magnum<br />
orientation relative to the orbital axis are<br />
hypothesized to be evolutionary adaptations<br />
to head posture during habitual locomotion,<br />
<strong>and</strong> appear necessary because of the limited<br />
range of motion at the atlanto-occipital joint<br />
(Graf et al., 1995).<br />
MAJOR UNRESOLVED ISSUES OF<br />
CRANIAL BASE VARIATION IN PRIMATE<br />
EVOLUTION<br />
Studies of <strong>cranial</strong> <strong>base</strong> variation in fossil<br />
<strong>primate</strong>s <strong>and</strong> hominins have been rare because<br />
this region of the skull is usually<br />
poorly preserved or destroyed in most fossils,<br />
<strong>and</strong> because it is hard to visualize or<br />
measure without radiographs or computed<br />
tomography (CT) scans. <strong>The</strong> coming years,<br />
however, are likely to see a renaissance of<br />
research on the role of the <strong>cranial</strong> <strong>base</strong> in<br />
<strong>primate</strong> <strong>cranial</strong> evolution as CT scans of<br />
fossils become more readily available. Here<br />
we review six major topics where future research<br />
on the <strong>cranial</strong> <strong>base</strong> in both fossil <strong>and</strong><br />
extant <strong>primate</strong>s promises to provide important<br />
insights: 1) the relationship between<br />
encephalization, circumorbital form, <strong>and</strong><br />
the origin of <strong>primate</strong>s; 2) the evolution of<br />
the integrated “facial block” in haplorhines;<br />
3) the determinants of basi<strong>cranial</strong> flexion in<br />
hominins; 4) the relationship between basi<strong>cranial</strong><br />
flexion <strong>and</strong> the shape of the vocal<br />
tract; 5) the role of the <strong>cranial</strong> <strong>base</strong> in facial<br />
retraction in Homo sapiens; <strong>and</strong> 6) the reliability<br />
of basi<strong>cranial</strong> characters as indicators<br />
of <strong>primate</strong> phylogeny.<br />
Primate origins, encephalization, <strong>and</strong><br />
circumorbital form<br />
<strong>The</strong> basicranium likely played a key role<br />
in the evolution of the unique configuration<br />
of the <strong>primate</strong> skull. Over the past three<br />
decades, the visual predation hypothesis<br />
(VPH) has become a well-accepted model of<br />
<strong>primate</strong> origins (Martin, 1990; Fleagle,<br />
1999). <strong>The</strong> VPH argues that the first <strong>primate</strong>s<br />
were nocturnal visual predators of<br />
small invertebrates <strong>and</strong> vertebrates, <strong>and</strong><br />
this required more anteriorly facing <strong>and</strong><br />
closely approximated orbital apertures<br />
(Cartmill, 1970, 1972, 1974, 1992). Increased<br />
orbital convergence enlarges the<br />
binocular field for greater stereoscopic vision<br />
<strong>and</strong> a clear retinal image for depth<br />
perception <strong>and</strong> prey location (Allman, 1977,<br />
1982). <strong>The</strong> VPH further posits that relatively<br />
larger orbits <strong>and</strong> grasping appendages<br />
with nails are adaptations to being<br />
nocturnal in an arboreal, terminal-branch<br />
setting (Cartmill, 1970, 1972, 1974, 1992;<br />
Kay <strong>and</strong> Cartmill, 1974, 1977; Dagosto,<br />
1988; Covert <strong>and</strong> Hamrick, 1993; Hamrick,<br />
1998, 1999; Lemelin, 1999). <strong>The</strong>se adaptations<br />
differ significantly from the <strong>cranial</strong><br />
<strong>and</strong> locomotor specializations of putative<br />
sister taxa such as plesiadapiforms <strong>and</strong> dermopterans<br />
(Cartmill, 1972, 1974, 1992; Kay<br />
<strong>and</strong> Cartmill, 1974, 1977; Beard, 1993; Ravosa<br />
et al., 2000a).<br />
According to the VPH, increased orbital<br />
convergence moves the orbital apertures out<br />
of the plane of the temporal fossa, a condition<br />
entailing greater ocular disruption during<br />
mastication (Cartmill, 1970, 1972, 1974,<br />
1992). A rigid postorbital bar may <strong>function</strong><br />
to stiffen the lateral orbital margins <strong>and</strong><br />
thus counter ocular deformation during biting<br />
<strong>and</strong> chewing to ensure a high level of<br />
stereoscopic acuity in an organism that processes<br />
food while hunting <strong>and</strong> foraging<br />
(Cartmill, 1970, 1972). This appears to be<br />
particularly important, given that strepsirhines<br />
with unfused symphyses have been<br />
shown to recruit relatively less balancingside<br />
than working-side adductor muscle<br />
force during unilateral mastication (Hyl<strong>and</strong>er<br />
et al., 1998, 2000). This differential<br />
muscle recruitment results in a pattern of<br />
lower strains along the balancing-side postorbital<br />
bar than the working-side postorbital<br />
bar (Ravosa et al., 2000a). Thus, an<br />
organism with a postorbital ligament <strong>and</strong> a<br />
stepsirhine-like adductor pattern (the latter<br />
of which is inferred for basal <strong>primate</strong>s <strong>base</strong>d<br />
on the presence of unfused symphyses; Ravosa,<br />
1996, 1999) would experience an<br />
asymmetrical circumorbital <strong>and</strong>, in turn, an<br />
ocular loading pattern that is hypothesized
152 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
to compromise effective stereoscopic visual<br />
acuity.<br />
Analyses of felids (perhaps the best analog<br />
for the skull of basal <strong>primate</strong>s), herpestids,<br />
<strong>and</strong> pteropodids demonstrate that<br />
postorbital bar formation characterizes taxa<br />
with increased orbital convergence <strong>and</strong>/or<br />
greater orbital frontation (Noble et al.,<br />
2000; Ravosa et al., 2000a). As both orbital<br />
characteristics became more developed during<br />
early <strong>primate</strong> evolution (Simons, 1962;<br />
Cartmill, 1970, 1972, 1974, 1992; Szalay et<br />
al., 1987; Martin, 1990; Fleagle, 1999), it is<br />
likely that <strong>primate</strong> postorbital bar development<br />
is correlated with both evolutionary<br />
transformations in the orbital complex (Ravosa<br />
et al., 2000a).<br />
<strong>The</strong> role of orbital frontation in postorbital<br />
bar formation is especially significant<br />
because it apparently reflects interactions<br />
among several factors unique to the early<br />
evolution of small <strong>primate</strong>s (Ravosa et al.,<br />
2000a). First among these factors is encephalization.<br />
Both early <strong>primate</strong>s <strong>and</strong> their putative<br />
ancestors were tiny, weighing between<br />
100–300 g (Kay <strong>and</strong> Cartmill, 1977;<br />
Dagosto, 1988; Martin, 1990; Beard, 1993;<br />
Covert <strong>and</strong> Hamrick, 1993; Fleagle, 1999).<br />
Thus, the greater encephalization of basal<br />
<strong>primate</strong>s (Martin, 1990) did not result from<br />
phyletic size decreases 7 (Gould, 1975; Shea,<br />
1987). Instead, increased relative brain size<br />
<strong>and</strong> orbital frontation appear linked to nocturnal<br />
visual predation (Ravosa et al.,<br />
2000a), which is related to increases in the<br />
relative size of the visual cortex (Cartmill,<br />
1974, 1992) <strong>and</strong> greater encephalization<br />
(Barton, 1998). This hypothesis complements<br />
prior claims that increased encephalization<br />
in basal <strong>primate</strong>s is related to the<br />
unique combination of arboreality, precociality,<br />
<strong>and</strong> small body size (Shea, 1987).<br />
Apart from being more encephalized than<br />
non<strong>primate</strong> archontans, the first <strong>primate</strong>s<br />
(<strong>and</strong> felids) possessed relatively larger eyes<br />
<strong>and</strong> more convergent orbits (Kay <strong>and</strong> Cartmill,<br />
1977; Martin, 1990; Covert <strong>and</strong> Hamrick,<br />
1993; Cartmill, 1992; Ravosa et al.,<br />
7 As phyletic dwarfs are more encephalized than like-sized<br />
sister taxa (Gould, 1975; Shea, 1987), presumably they are also<br />
more flexed, highlighting the complex relationships between<br />
brain evolution <strong>and</strong> changes in basi<strong>cranial</strong> <strong>and</strong> facial form.<br />
2000a). This combination of derived features<br />
creates a spatial packing problem in<br />
which the position of the frontal lobes <strong>and</strong><br />
anterior <strong>cranial</strong> fossa have a major influence<br />
on orbital aperture orientation, integrating<br />
morphological variation in these adjacent<br />
<strong>cranial</strong> regions (see above). Because<br />
neural <strong>and</strong> ocular size scale with negative<br />
allometry (Schultz, 1940; Gould, 1975), this<br />
structural constraint would be particularly<br />
marked in smaller, <strong>and</strong> thus more frontated,<br />
taxa—the morphospace in which<br />
basal <strong>primate</strong>s <strong>and</strong> felids happen to develop<br />
postorbital bars.<br />
Anthropoid origins <strong>and</strong> <strong>cranial</strong><br />
<strong>base</strong>-face interactions<br />
Another interesting problem is the role of<br />
the <strong>cranial</strong> <strong>base</strong> in the fundamental rearrangement<br />
of the face along the stem lineage<br />
leading to haplorhines <strong>and</strong> anthropoids.<br />
<strong>The</strong>se changes include: increased<br />
orbital convergence <strong>and</strong> frontation; increased<br />
relative brain size, especially in the<br />
frontal <strong>and</strong> temporal lobes; a more acutely<br />
angled (flexed) <strong>cranial</strong> <strong>base</strong>; partial retraction<br />
of the face below the braincase; reduction<br />
of the olfactory apparatus <strong>and</strong><br />
interorbital region with concomitant<br />
approximation of the orbits; relatively<br />
smaller orbits associated with diurnality;<br />
<strong>and</strong> the presence of a postorbital septum<br />
(Cartmill, 1970, 1980; Radinsky, 1968,<br />
1979; Rosenberger, 1985, 1986; Ravosa,<br />
1991b; Ross <strong>and</strong> Ravosa, 1993; Ross,<br />
1995a,b). Not surprisingly, changes in <strong>cranial</strong><br />
<strong>base</strong> shape have been key features of all<br />
the models proposed to explain the order in<br />
which these features arose, their putative<br />
<strong>function</strong>s, <strong>and</strong> their interactions. According<br />
to Cartmill (1970), the fundamental difference<br />
between haplorhines <strong>and</strong> strepsirhines<br />
centers on whether orbital convergence occurs<br />
towards the top of the skull or at the<br />
front. If, as in haplorhines, the orbits converge<br />
anteriorly (associated with increased<br />
orbital frontation), then the orbits not only<br />
compress the olfactory region, reducing its<br />
dimensions, but also become closely approximated<br />
to the midline anterior <strong>cranial</strong> <strong>base</strong>.<br />
This necessarily reduces the size of the olfactory<br />
apparatus <strong>and</strong> forms an interorbital<br />
septum, facilitating a subsequent increase
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 153<br />
in relative encephalization by expansion of<br />
the brain forward over the top of the orbits.<br />
It has been argued that, as predicted by<br />
Dabelow (1931), by bringing the orbits <strong>and</strong><br />
anterior <strong>cranial</strong> <strong>base</strong> into close continuity,<br />
they became structurally integrated such<br />
that changes in the orientation of one necessarily<br />
affect the other (Ross <strong>and</strong> Ravosa,<br />
1993). Small nocturnal strepsirhines, in<br />
contrast, tend to converge their orbits towards<br />
the top of their head, not compressing<br />
the olfactory apparatus, <strong>and</strong> preventing<br />
brain expansion over the orbits concomitant<br />
with a shift to diurnality. <strong>The</strong> orbits <strong>and</strong><br />
anterior <strong>cranial</strong> <strong>base</strong> in all strepsirhines are<br />
not as unified structurally, <strong>and</strong> thus basi<strong>cranial</strong><br />
flexion <strong>and</strong> orbit orientation do not<br />
covary as greatly.<br />
<strong>The</strong> evidence that all omomyiforms that<br />
are well enough preserved have an interorbital<br />
septum below the olfactory tract, like<br />
that of Tarsius <strong>and</strong> small anthropoids (Ross,<br />
1994), suggests that this integration of anterior<br />
<strong>cranial</strong> <strong>base</strong> <strong>and</strong> upper face may be an<br />
early unique derived feature of the haplorhine<br />
stem lineage. This integration set the<br />
stage for the subsequent evolution of the<br />
haplorhine postorbital septum. Increased<br />
orbital frontation (klinorhynchy) <strong>and</strong> convergence<br />
in early anthropoids caused the<br />
anterior temporal muscles <strong>and</strong> orbit to come<br />
into close proximity, leading to the evolution<br />
of a postorbital septum (Ross, 1995b, 1996).<br />
Exactly why increased frontation occurred<br />
in haplorhines remains unexplained, although<br />
it has been argued that increased<br />
relative brain size might have caused increased<br />
basi<strong>cranial</strong> flexion, producing increased<br />
orbital frontation as a consequence<br />
of the integration of the anterior <strong>cranial</strong><br />
<strong>base</strong> <strong>and</strong> orbits (Ross, 1996; see also Ravosa<br />
et al., 2000a on the effects of small size on<br />
skull form in basal <strong>primate</strong>s). This hypothesis<br />
remains to be evaluated in fossil stem<br />
anthropoids for want of well-preserved specimens,<br />
but is not supported by the fact that<br />
early anthropoids had a postorbital septum<br />
in conjunction with relatively small brains<br />
(Ross, 2000). It remains to be determined<br />
why the haplorhine stem lineage evolved<br />
more frontated orbits, but the findings of<br />
Strait <strong>and</strong> Ross (1999) suggest that the role<br />
of posture should be considered.<br />
Variation in hominin <strong>cranial</strong> <strong>base</strong> angle<br />
How to account for variation in basi<strong>cranial</strong><br />
flexion in hominins has been controversial<br />
<strong>and</strong> remains unresolved. Several recent<br />
studies (e.g., Ross <strong>and</strong> Henneberg, 1995;<br />
Spoor, 1997) have shown that the <strong>cranial</strong><br />
<strong>base</strong> in Australopithecus <strong>and</strong> Homo is generally<br />
more flexed than in Pan or other nonhuman<br />
<strong>primate</strong>s. This difference raises two<br />
questions. First, how much is <strong>cranial</strong> <strong>base</strong><br />
flexion among early hominins related to upright<br />
posture, facial orientation, or brain<br />
size? Second, what factors account for the<br />
observed variation in <strong>cranial</strong> <strong>base</strong> angle<br />
among hominins?<br />
Although <strong>cranial</strong> <strong>base</strong> angles vary substantially<br />
among hominin species, australopithecines<br />
have CBAs generally intermediate<br />
between humans <strong>and</strong> chimpanzees, but<br />
with more flexed <strong>cranial</strong> <strong>base</strong>s among A.<br />
boisei <strong>and</strong> less flexed <strong>cranial</strong> <strong>base</strong>s for A.<br />
aethiopicus (KNM-WT 17000) (F. Spoor,<br />
personal communication). Until now, the<br />
hypothesis that <strong>cranial</strong> <strong>base</strong> flexion in hominins<br />
is an adaptation for increased brain<br />
size relative to basi<strong>cranial</strong> length (Gould,<br />
1977) has received the most support (Ross<br />
<strong>and</strong> Ravosa, 1993; Ross <strong>and</strong> Henneberg,<br />
1995; Spoor, 1997; McCarthy, 2001). In particular,<br />
if one measures IRE5 vs. CBA1<br />
(thereby including the cribriform plate in<br />
measures of both basi<strong>cranial</strong> length <strong>and</strong> the<br />
angle of the <strong>cranial</strong> <strong>base</strong>), then H. sapiens<br />
<strong>and</strong> other hominin taxa such as A. africanus<br />
have exactly the degree of flexion expected<br />
by basi<strong>cranial</strong> length.<br />
However, not all of the variation in hominin<br />
CBA can be explained by relative brain<br />
size. For example, Ne<strong>and</strong>erthals <strong>and</strong> archaic<br />
Homo fossils such as Kabwe have considerably<br />
more extended CBA1s than H. sapiens<br />
(about 15°), even though they are<br />
bipedal <strong>and</strong> similarly encephalized (Ruff et<br />
al., 1997). In addition, other measures of<br />
<strong>cranial</strong> <strong>base</strong> angle <strong>and</strong> relative encephalization,<br />
which do not include the cribriform<br />
plate (CBA4 <strong>and</strong> IRE5), indicate that H.<br />
sapiens have less flexed <strong>cranial</strong> <strong>base</strong>s then<br />
expected for anthropoids of their size (Ross<br />
<strong>and</strong> Henneberg, 1995). This finding highlights<br />
the likelihood that no single explanation<br />
will account for interspecific differences
154 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
in CBA among hominins. Other factors that<br />
have been argued to contribute to variation<br />
in CBA, including facial kyphosis <strong>and</strong> head<br />
<strong>and</strong> neck posture, cannot be shown to be<br />
important correlates of basi<strong>cranial</strong> flexion.<br />
Most importantly, the comparative study by<br />
Strait <strong>and</strong> Ross (1999) of CBA, head-neck<br />
angle, <strong>and</strong> orbital axis orientation among<br />
extant <strong>primate</strong>s found that basi<strong>cranial</strong> flexion<br />
is primarily influenced by relative brain<br />
size <strong>and</strong> not head <strong>and</strong> neck posture. <strong>The</strong><br />
traditional view that human basi<strong>cranial</strong><br />
flexion is somehow an adaptation for orthograde<br />
posture is no longer tenable.<br />
Cranial <strong>base</strong> flexion <strong>and</strong> vocal tract<br />
shape in hominins<br />
Flexion of the <strong>cranial</strong> <strong>base</strong> has been argued<br />
to be an important correlate of the<br />
shape of the vocal tract. In particular, several<br />
researchers (Lieberman et al., 1972,<br />
1992; Laitman <strong>and</strong> Crelin, 1976; Laitman et<br />
al., 1978, 1979; Laitman <strong>and</strong> Heimbuch,<br />
1982) claimed that the degree of flexion of<br />
the external <strong>cranial</strong> <strong>base</strong> (between the inferior<br />
aspect of the basioccipital clivus <strong>and</strong> the<br />
palate) influences the position of the hyolaryngeal<br />
complex. In most mammals, the<br />
hyoid <strong>and</strong> larynx lie close to the soft palate<br />
so that the epiglottis <strong>and</strong> soft palate can<br />
engage, permitting simultaneous breathing<br />
<strong>and</strong> swallowing (Laitman <strong>and</strong> Reidenberg,<br />
1993; German et al., 1996; Larson <strong>and</strong> Herring,<br />
1996; Crompton et al., 1997). In contrast,<br />
humans have a uniquely shaped pharynx<br />
in which the hyo-laryngeal complex<br />
descends inferiorly relative to the oral cavity,<br />
causing the soft palate <strong>and</strong> epiglottis to<br />
become disengaged so that the trachea <strong>and</strong><br />
esophagus share a common passageway<br />
(Negus, 1949; Crelin, 1973). Hyo-laryngeal<br />
descent is an important physiological basis<br />
for many aspects of human speech. Flexion<br />
of the external <strong>cranial</strong> <strong>base</strong> in combination<br />
with a low position of the larynx relative to<br />
the palate divide the human vocal tract (VT)<br />
into separate horizontal <strong>and</strong> vertical “tubes”<br />
of approximately equal length, whose crosssectional<br />
areas can be modified independently<br />
at least tenfold by the tongue<br />
(Stevens <strong>and</strong> House, 1955; Fant, 1960;<br />
Stevens, 1972; Baer et al., 1991). Dynamic<br />
filtering in the two-tube human VT <strong>function</strong>s<br />
to produce a wide range of vowels<br />
whose formant frequencies are acoustically<br />
distinct regardless of vocal tract length<br />
(Fant, 1960; Nearey, 1978; Lieberman,<br />
1984; Carre et al., 1994; Beckman et al.,<br />
1995).<br />
Although the speech-related acoustical<br />
properties of the unique human vocal tract<br />
are not in dispute, the role of <strong>cranial</strong> <strong>base</strong><br />
flexion in hyo-laryngeal descent is controversial,<br />
yet potentially important for reconstructing<br />
the anatomy of the vocal tract in<br />
fossil hominins Two questions are of special<br />
importance. First, what is the relationship<br />
of external <strong>cranial</strong> <strong>base</strong> flexion to the descent<br />
<strong>and</strong>/or positioning of the hyoid relative<br />
to the oral cavity? Second, how does the<br />
angle of the external <strong>cranial</strong> <strong>base</strong> change<br />
during development, <strong>and</strong> what is its relationship<br />
to internal <strong>cranial</strong> <strong>base</strong> angle?<br />
<strong>The</strong> original hypothesis that flexion of the<br />
external <strong>cranial</strong> <strong>base</strong> in humans contributes<br />
to laryngeal descent, <strong>and</strong> thus can be used<br />
to reconstruct the vocal tract of fossil hominins<br />
(Lieberman <strong>and</strong> Crelin, 1971; Lieberman<br />
et al., 1972; Laitman <strong>and</strong> Crelin, 1976;<br />
Laitman <strong>and</strong> Heimbuch, 1982; Lieberman,<br />
1984), was <strong>base</strong>d on three observations.<br />
First, these researchers inferred a relationship<br />
between <strong>cranial</strong> <strong>base</strong> flexion <strong>and</strong> laryngeal<br />
descent on the basis of comparisons of<br />
neonatal <strong>and</strong> adult humans vs. nonhuman<br />
<strong>primate</strong>s. In particular, human neonates,<br />
like nonhuman <strong>primate</strong> adults, have a relatively<br />
extended <strong>cranial</strong> <strong>base</strong> <strong>and</strong> a high hyoid,<br />
whereas only human adults have both a<br />
flexed <strong>cranial</strong> <strong>base</strong> <strong>and</strong> a descended larynx.<br />
Second, internal <strong>and</strong> external basi<strong>cranial</strong><br />
flexion were believed to covary with the descent<br />
of the larynx (George, 1978). Third,<br />
external <strong>cranial</strong> <strong>base</strong> flexion was believed to<br />
reorient the suprahyoid muscles <strong>and</strong> ligaments<br />
more vertically, <strong>and</strong> to shorten the<br />
antero-posterior length of the oropharynx<br />
between the palate <strong>and</strong> the cervical vertebrae,<br />
thus requiring the larynx <strong>and</strong> posterior<br />
tongue to be positioned lower relative to<br />
the hard palate.<br />
Lieberman <strong>and</strong> McCarthy (1999) tested<br />
the relationship between <strong>cranial</strong> <strong>base</strong> flexion<br />
<strong>and</strong> hyo-laryngeal position using a longitudinal<br />
series of radiographs in humans<br />
(the Denver Growth Study), which pre-
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 155<br />
Fig. 16. Longitudinal changes in the angle of the<br />
external <strong>cranial</strong> <strong>base</strong> (CBA5 from basion-sphenobasionhormion)<br />
<strong>and</strong> the height of the vocal tract (the distance<br />
from the vocal folds to the plane of the hard palate,<br />
perpendicular to the posterior pharyngeal wall). Data<br />
are from a longitudinal study of growth in 15 males <strong>and</strong><br />
13 females (for details, see Lieberman <strong>and</strong> McCarthy,<br />
1999). Note that the height of the vocal tract continues<br />
to grow throughout the somatic growth period, whereas<br />
the external <strong>cranial</strong> <strong>base</strong> angle ceases to change appreciably<br />
after approximately 3 postnatal years.<br />
served details of larynx <strong>and</strong> hyoid position<br />
in upright subjects x-rayed during quiet respiration.<br />
This study found no statistically<br />
significant relationship between either internal<br />
or external <strong>cranial</strong> <strong>base</strong> flexion <strong>and</strong><br />
hyo-laryngeal descent. As Figure 16 shows,<br />
the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> the position of the larynx<br />
must be partially independent in humans<br />
because the <strong>cranial</strong> <strong>base</strong> flexes rapidly<br />
during the first few years after birth,<br />
whereas the larynx <strong>and</strong> hyoid descend gradually<br />
until the end of the adolescent growth<br />
spurt. Consequently, the flexion of the external<br />
<strong>cranial</strong> <strong>base</strong> (<strong>and</strong> presumably its effects<br />
on suprahyoid muscle orientation) cannot<br />
be used to infer vocal tract dimensions<br />
in fossil hominins (Lieberman et al., 1998).<br />
Similarly, Chan (1991) demonstrated that<br />
the correlation between styloid process orientation<br />
<strong>and</strong> laryngeal position is not strong<br />
enough to estimate vocal tract dimensions<br />
reliably.<br />
External flexion has been measured in<br />
several ways, all of which suggest that external<br />
<strong>and</strong> internal <strong>cranial</strong> <strong>base</strong> angles are<br />
correlated with each other, but differ in<br />
their pattern of growth in humans <strong>and</strong> nonhuman<br />
<strong>primate</strong>s. Laitman et al. (1976,<br />
1978, 1979, 1982) developed a composite,<br />
size-corrected measure of exo<strong>cranial</strong> flexion<br />
between the basioccipital <strong>and</strong> the palate,<br />
which they measured on cross-sectional<br />
samples of humans, apes, monkeys, <strong>and</strong><br />
several fossil hominins. More recently,<br />
Lieberman <strong>and</strong> McCarthy (1999) measured<br />
external <strong>cranial</strong> <strong>base</strong> flexion in a longitudinal<br />
sample of humans using two lines, one<br />
extending from basion to sphenobasion, <strong>and</strong><br />
the second from sphenobasion to hormion.<br />
May <strong>and</strong> Sheffer (1999) took essentially the<br />
same measurement on cross-sectional samples<br />
of humans, chimpanzees, gorillas, <strong>and</strong><br />
several fossil hominins. <strong>The</strong>se studies all<br />
agree that flexion of the internal <strong>cranial</strong>
156 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
<strong>base</strong> in humans occurs prior to the eruption<br />
of the first permanent molars <strong>and</strong> then remains<br />
stable, but that the external <strong>cranial</strong><br />
<strong>base</strong> extends gradually in all nonhuman <strong>primate</strong>s<br />
throughout the period of facial<br />
growth. 8 Moreover, the patterns of external<br />
<strong>and</strong> internal <strong>cranial</strong> <strong>base</strong> angulation mirror<br />
each other. <strong>The</strong> internal <strong>cranial</strong> <strong>base</strong> (measured<br />
using both Ba-S-FC <strong>and</strong> L<strong>and</strong>zert’s<br />
angle) flexes in humans rapidly prior to 2<br />
postnatal years <strong>and</strong> then remains stable,<br />
but extends in nonhuman <strong>primate</strong>s gradually<br />
throughout the period of facial growth<br />
(Fig. 7) (Lieberman <strong>and</strong> McCarthy, 1999).<br />
Cranial <strong>base</strong> shape <strong>and</strong> facial<br />
projection in Homo<br />
Although the effects of <strong>cranial</strong> <strong>base</strong> angulation<br />
on the angle of the face relative to the<br />
rest of the skull (facial kyphosis) have long<br />
been the subject of much research (see<br />
above), there has been recent interest in the<br />
role of the <strong>cranial</strong> <strong>base</strong> on facial projection.<br />
Facial projection (which is a more general<br />
term for neuro-orbital disjunction) is defined<br />
here as the extent to which the nonrostral<br />
portion of the face is positioned anteriorly<br />
relative to the foramen caecum, the<br />
most antero-inferior point on the <strong>cranial</strong><br />
<strong>base</strong> (note that facial projection <strong>and</strong> prognathism<br />
are different). Variation in facial<br />
projection, along with an underst<strong>and</strong>ing of<br />
their developmental <strong>base</strong>s, may be important<br />
for testing hypotheses about recent<br />
hominin evolution. In particular, Lieberman<br />
(1995, 1998, 2000) has argued that<br />
variation in facial projection accounts for<br />
many of the major differences in overall<br />
craniofacial form between H. sapiens <strong>and</strong><br />
other closely-related “archaic” Homo taxa,<br />
including the Ne<strong>and</strong>erthals. Whereas all<br />
nonextant hominins have projecting faces,<br />
“anatomically modern” H. sapiens is<br />
uniquely characterized by a retracted facial<br />
profile in which the majority of the face lies<br />
beneath the braincase (Weidenreich, 1941;<br />
Moss <strong>and</strong> Young, 1960; Vinyard, 1994;<br />
Lieberman, 1995, 1998; Vinyard <strong>and</strong> Smith,<br />
1997; May <strong>and</strong> Sheffer, 1999; Ravosa et al.,<br />
2000b). As a consequence, H. sapiens also<br />
has a more vertical frontal profile, less projecting<br />
browridges, a rounder overall <strong>cranial</strong><br />
shape, <strong>and</strong> a relatively shorter oropharyngeal<br />
space between the back of the hard<br />
palate <strong>and</strong> the foramen magnum—virtually<br />
all of the supposed autapomorphies of “anatomically<br />
modern” H. sapiens.<br />
What is the role of the <strong>cranial</strong> <strong>base</strong> in<br />
facial projection? Lieberman (1998, 2000)<br />
proposed that four independent factors account<br />
for variation in facial projection: 1)<br />
antero-posterior facial length, 2) anterior<br />
<strong>cranial</strong> <strong>base</strong> length, 3) <strong>cranial</strong> <strong>base</strong> angle,<br />
<strong>and</strong> 4) the antero-posterior length of the<br />
middle <strong>cranial</strong> fossa from sella to PM<br />
plane. 9 Each of these variables has a different<br />
growth pattern, but combine to influence<br />
the position of the face relative to the<br />
basicranium <strong>and</strong> neurocranium. For example,<br />
facial projection can occur through having<br />
a long face relative to a short anterior<br />
<strong>cranial</strong> fossa, a long middle <strong>cranial</strong> fossa<br />
relative to the length of the anterior <strong>cranial</strong><br />
fossa, <strong>and</strong>/or a more extended <strong>cranial</strong> <strong>base</strong>.<br />
Partial correlation analyses of cross-sectional<br />
samples of Homo sapiens <strong>and</strong> Pan<br />
troglodytes indicate that each contributes<br />
significantly to the <strong>ontogeny</strong> of facial projection<br />
in humans <strong>and</strong> apes when the associations<br />
between these variables <strong>and</strong> with<br />
overall <strong>cranial</strong> length <strong>and</strong> endo<strong>cranial</strong> volume<br />
as well as other <strong>cranial</strong> dimensions are<br />
held constant (Lieberman, 2000). In other<br />
words, chimpanzees <strong>and</strong> humans with relatively<br />
longer faces, shorter anterior <strong>cranial</strong><br />
<strong>base</strong>s, less flexed <strong>cranial</strong> <strong>base</strong>s, <strong>and</strong>/or<br />
longer middle <strong>cranial</strong> fossae tend to have<br />
relatively more projecting faces.<br />
In an analysis of radiographs of fossil<br />
hominins, Lieberman (1998) argued that<br />
the major cause for facial retraction <strong>and</strong> its<br />
resulting effects on modern human <strong>cranial</strong><br />
shape was a change in the <strong>cranial</strong> <strong>base</strong><br />
rather than the face itself. Specifically, middle<br />
<strong>cranial</strong> fossa length (termed ASL) was<br />
estimated to be approximately 25% shorter<br />
in anatomically modern humans, both re-<br />
8 May <strong>and</strong> Sheffer (1999) did not find evidence for postnatal<br />
extension of the <strong>cranial</strong> <strong>base</strong> in Pan, largely because of insufficient<br />
sample sizes that were divided into overly large ontogenetic<br />
stages.<br />
9 This dimension was originally termed anterior sphenoid<br />
length (ASL), but it is really a measure of the midline prechordal<br />
length of the middle <strong>cranial</strong> fossa (Lieberman, 2000).
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 157<br />
Fig. 17. Thin-plate spline analysis of an Australian male (from Queensl<strong>and</strong>) relative to Kabwe 1<br />
(target). Eighteen l<strong>and</strong>marks from each skull were initially superimposed using a resistant-fit Procrustes<br />
analysis. <strong>The</strong> deformation grid shows that the archaic Homo fossil has a relatively more projecting <strong>and</strong><br />
taller face, a more extended <strong>cranial</strong> <strong>base</strong>, a relatively shorter middle <strong>cranial</strong> fossa, <strong>and</strong> a relatively longer<br />
pharyngeal space between the palate <strong>and</strong> the foramen magnum.<br />
cent <strong>and</strong> Pleistocene, than in Ne<strong>and</strong>erthals<br />
<strong>and</strong> other taxa of archaic Homo, whereas<br />
anterior <strong>cranial</strong> <strong>base</strong> length <strong>and</strong> facial<br />
length were not significantly different between<br />
these taxa.<br />
Lieberman (1998), however, incorrectly<br />
measured ASL in the few archaic humans in<br />
which the <strong>cranial</strong> <strong>base</strong> is well preserved. As<br />
shown by Spoor et al. (1999), ASL is not<br />
significantly longer in archaic Homo than in<br />
modern humans, but the angle of the <strong>cranial</strong><br />
<strong>base</strong> (CBA1) is about 15° more extended<br />
in archaic Homo fossils such as Gibraltar,<br />
Monte Circeo, <strong>and</strong> Kabwe than in samples<br />
of Pleistocene <strong>and</strong> recent modern humans<br />
(P 0.05). Consequently, Spoor et al. (1999)<br />
<strong>and</strong> Lieberman (2000) concluded that differences<br />
in <strong>cranial</strong> <strong>base</strong> angle are more likely<br />
to account for facial retraction in modern<br />
humans, as well as for other differences<br />
noted by Lieberman (1998), such as the relatively<br />
shorter pharynx behind the palate.<br />
This hypothesis needs to be tested carefully,<br />
but is explored here in a preliminary fashion<br />
with a geometric morphometric analysis<br />
comparing the shape of the Kabwe cranium<br />
with a large, robust recent H. sapiens (a<br />
male Australian). Figure 17 shows a thinplate<br />
spline transformation of the Australian<br />
into Kabwe (computed using Mor-
158 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
phometrika, version 0.007, Jeff Walker,<br />
Chicago, IL), <strong>base</strong>d on an initial resistant-fit<br />
superimposition Procrustes analysis of six<br />
<strong>cranial</strong> <strong>base</strong> l<strong>and</strong>marks, seven facial l<strong>and</strong>marks,<br />
<strong>and</strong> five neuro<strong>cranial</strong> l<strong>and</strong>marks. 10<br />
<strong>The</strong> thin-plate spline, which is <strong>base</strong>d on a<br />
Procrustes analysis that geometrically corrects<br />
for most effects of size differences,<br />
shows that Kabwe has a considerably more<br />
projecting face (i.e., between nasion <strong>and</strong> the<br />
foramen caecum) in conjunction with a relatively<br />
more extended <strong>cranial</strong> <strong>base</strong> (14 o ), a<br />
dorsally rotated PM plane relative to the<br />
posterior <strong>cranial</strong> <strong>base</strong>, <strong>and</strong> a relatively<br />
longer pharyngeal space between the maxilla<br />
<strong>and</strong> the foramen magnum. In addition,<br />
when one examines specific, size-corrected<br />
dimensions (st<strong>and</strong>ardized by the geometric<br />
mean of all the interl<strong>and</strong>mark distances),<br />
midfacial length (PM-Na) is 19% longer in<br />
Kabwe than in the Australian modern individual,<br />
but the length of the anterior <strong>cranial</strong><br />
<strong>base</strong> (S-FC) is only 4% shorter. In other<br />
words, Kabwe exhibits a considerably more<br />
projecting face than the H. sapiens specimen<br />
because it has a more extended <strong>cranial</strong><br />
<strong>base</strong> in conjunction with a relatively longer<br />
face. Changes in middle <strong>cranial</strong> fossa shape,<br />
therefore, appear to have had major effects<br />
on facial retraction in human evolution, but<br />
need to be further examined using additional<br />
specimens.<br />
Additional, intriguing evidence that the<br />
<strong>cranial</strong> <strong>base</strong> can play an important role in<br />
facial retraction may be come from studies<br />
of craniofacial growth abnormalities <strong>and</strong><br />
from laboratory studies of mice. Mice that<br />
are homozygous-recessive for the retrognathic<br />
Brachyrrhine (Br) allele are characterized<br />
by a primary growth defect in the<br />
anterior <strong>cranial</strong> <strong>base</strong> (Beechey et al., 1998;<br />
Ma <strong>and</strong> Lozanoff, 1999) that leads to a severely<br />
retrognathic midfacial profile but a<br />
morphologically normal nasal septum <strong>and</strong><br />
face (Lozanoff, 1993; Lozanoff et al., 1994;<br />
10 <strong>The</strong>se l<strong>and</strong>marks are: basion, sella, pituitary point, sphenoidale,<br />
PMp (the anteriormost point on the greater wings of the<br />
sphenoid), foramen caecum, nasion, ANS, PNS, prosthion, maxillary<br />
tuberosities, fronton, orbitale, opisthocranion, the superior-most<br />
point on the vault, fronton, the inferior-most point on<br />
the supratoral sulcus, glabella. Resistant fit superimposition<br />
was used in order to minimize effects of the very different shape<br />
of the neurocranium in archaic Homo vs. modern H. sapiens.<br />
Ma <strong>and</strong> Lozanoff, 1999). <strong>The</strong> extent to<br />
which the morphological differences between<br />
the retrognathic Br mouse <strong>and</strong> controls<br />
is at all similar to the differences evident<br />
between H. sapiens <strong>and</strong> archaic Homo<br />
has yet to be determined. However, these<br />
studies, in conjunction with facial growth<br />
defects caused by chondrogenic growth disorders<br />
such as Crouzon syndrome, Pierre-<br />
Robin syndrome, <strong>and</strong> Down syndrome, highlight<br />
the important role the <strong>cranial</strong> <strong>base</strong><br />
plays in facial growth <strong>and</strong> integration (David<br />
et al., 1989).<br />
Cranial <strong>base</strong> characters in phylogenetic<br />
analyses<br />
One final consideration of interest is<br />
whether it might be profitable to focus on<br />
characters from the <strong>cranial</strong> <strong>base</strong> in taxonomic<br />
<strong>and</strong> phylogenetic analyses of <strong>primate</strong>s.<br />
This possibility has been raised by a<br />
number of authors (e.g., Olson, 1985; Shea,<br />
1985a, 1988; Lieberman et al., 1996; Lieberman,<br />
1997; Strait et al., 1997; Strait, 1998)<br />
for three reasons. First, the <strong>cranial</strong> <strong>base</strong><br />
derives from endochrondral precursors<br />
rather than though intramembranous ossification<br />
processes (endochondral bones are<br />
thought to have more direct genetic influence<br />
in terms of initial shape); second, the<br />
<strong>cranial</strong> <strong>base</strong> is the first part of the skull to<br />
reach adult size <strong>and</strong> shape (Moore <strong>and</strong><br />
Lavelle, 1974); <strong>and</strong> third, the <strong>cranial</strong> <strong>base</strong><br />
may play a greater role in influencing facial<br />
shape than vice versa (see above). Consequently,<br />
one might expect <strong>cranial</strong> <strong>base</strong> characters<br />
to preserve more phylogenetic signal<br />
than facial characters by virtue of being<br />
more heritable <strong>and</strong> less influenced by the<br />
epigenetic responses to external influences<br />
during postnatal <strong>ontogeny</strong> rampant in the<br />
facial skeleton (Herring, 1993).<br />
Expectations aside, there are currently no<br />
data suggesting that the basicranium is actually<br />
a better source of characters than<br />
other regions of the skull for phylogenetic<br />
analyses. In terms of narrow-sense heritability<br />
(h 2 ), basi<strong>cranial</strong>, neuro<strong>cranial</strong>, <strong>and</strong> facial<br />
characters have similar levels of heritability<br />
among <strong>primate</strong>s (Sjøvold, 1984;<br />
Cheverud <strong>and</strong> Buikstra, 1982; Cheverud,<br />
1995). In addition, basi<strong>cranial</strong> variables appear<br />
to be equally well (or poorly) correlated
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 159<br />
with other dimensions or features in hominoids<br />
(Strait, 1998), <strong>and</strong> in the human skull<br />
(Lieberman et al., 2000). Finally, those few<br />
studies that have focused on <strong>cranial</strong> <strong>base</strong><br />
characters do not yield results substantially<br />
different from analyses that incorporate<br />
other craniodental characters. Lieberman et<br />
al. (1996) found that basi<strong>cranial</strong> <strong>and</strong> vault<br />
characters tend to yield similar cladograms<br />
that differ only slightly from cladograms<br />
<strong>base</strong>d on facial characters. Strait et al.<br />
(1997) did not specifically examine characters<br />
from the <strong>cranial</strong> <strong>base</strong>, but found no<br />
major difference between trees <strong>base</strong>d on<br />
masticatory characters vs. those that were<br />
predominantly neuro<strong>cranial</strong> <strong>and</strong> basi<strong>cranial</strong>.<br />
In their study of <strong>primate</strong> higher taxonomic<br />
relationships, Ross et al. (1998) found<br />
the <strong>cranial</strong> data, consisting primarily of basi<strong>cranial</strong><br />
traits, to yield trees similar to<br />
those produced by the dental data, although<br />
with better resolution at older nodes. Thus,<br />
whether the basicranium is a better source<br />
of phylogenetic data remains open to question.<br />
<strong>The</strong> <strong>cranial</strong> <strong>base</strong> may be a good place to<br />
look for reliable characters if researchers<br />
are to focus on characters that describe developmental<br />
processes or events (e.g., flexion<br />
vs. extension at the spheno-occipital<br />
synchondrosis) rather than using characters<br />
that solely describe morphological variation<br />
(e.g., the angle of the whole <strong>cranial</strong><br />
<strong>base</strong>) (Hall, 1994; Lieberman, 1999). This<br />
hypothesis, however, has yet to be tested.<br />
<strong>The</strong> above studies, however, raise another<br />
key issue relevant to phylogenetic studies:<br />
the problem of independence. Cladistic<br />
analyses explicitly require one to use independent<br />
characters to avoid problems of<br />
convergent <strong>and</strong> correlated characters incorrectly<br />
biasing the outcome of any parsimony<br />
analysis. Yet the above studies demonstrate<br />
the existence of multiple <strong>and</strong> complicated<br />
interactions between the <strong>cranial</strong> <strong>base</strong> <strong>and</strong><br />
the neurocranium <strong>and</strong> between the <strong>cranial</strong><br />
<strong>base</strong> <strong>and</strong> the face. For example, variations<br />
in orbit size <strong>and</strong> orientation are linked to<br />
variations in the angle of the <strong>cranial</strong> <strong>base</strong>,<br />
brain size, <strong>and</strong> the orientation of the face<br />
relative to the rest of the skull. Many of<br />
these features have been treated as independent<br />
characters in recent cladistic analyses<br />
(e.g., Strait et al, 1997), but their effect<br />
on the results has yet to be determined.<br />
Further study of these interactions is<br />
needed to improve the reliability of phylogenetic<br />
analyses, <strong>and</strong> again highlight the need<br />
to consider morphological characters in<br />
terms of their generative processes (e.g.,<br />
Gould, 1977; Cheverud, 1982; Shea, 1985b;<br />
Hall, 1994; Lieberman, 1999).<br />
CONCLUSIONS<br />
Since the last major reviews of <strong>cranial</strong><br />
<strong>base</strong> anatomy in <strong>primate</strong>s (Scott, 1958;<br />
Moore <strong>and</strong> Lavelle, 1974; Sirianni <strong>and</strong><br />
Swindler, 1979), there has been a tremendous<br />
increase in our knowledge of chondro<strong>cranial</strong><br />
embryology, the patterns <strong>and</strong> processes<br />
of basi<strong>cranial</strong> growth, <strong>and</strong> the nature<br />
of basi<strong>cranial</strong> variation across <strong>primate</strong>s.<br />
Major advances include details of the morphogenetic<br />
independence between the prechordal<br />
<strong>and</strong> postchordal portions of the<br />
chondrocranium; comparative data on the<br />
relative importance of brain size, orbital orientation,<br />
facial orientation, <strong>and</strong> posture as<br />
factors that account for variation in <strong>cranial</strong><br />
<strong>base</strong> angulation; <strong>and</strong> ontogenetic <strong>and</strong> comparative<br />
data on the structural relationships<br />
between the anterior <strong>cranial</strong> <strong>base</strong> <strong>and</strong><br />
upper face in haplorhines vs. strepsirhines,<br />
<strong>and</strong> their influences on facial form. Despite<br />
these advances, many aspects of <strong>cranial</strong><br />
<strong>base</strong> growth, variation, <strong>and</strong> <strong>function</strong> remain<br />
poorly understood. For example, we do not<br />
know what ontogenetic processes govern<br />
flexion <strong>and</strong> extension of the <strong>cranial</strong> <strong>base</strong>, or<br />
which synchondroses are active in <strong>cranial</strong><br />
<strong>base</strong> elongation vs. angulation in humans<br />
<strong>and</strong> other <strong>primate</strong>s. Future research needs<br />
to be aimed at studying these processes as<br />
they relate to <strong>cranial</strong> shape, <strong>function</strong>, <strong>and</strong><br />
evolution.<br />
To conclude, we highlight two important<br />
practical <strong>and</strong> theoretical issues which we<br />
believe merit special consideration, <strong>and</strong><br />
which promise to further our underst<strong>and</strong>ing<br />
of craniofacial growth <strong>and</strong> variation. First,<br />
what are the major factors that generate<br />
variation in the <strong>cranial</strong> <strong>base</strong> among <strong>primate</strong>s?<br />
Second, to what extent does the <strong>cranial</strong><br />
<strong>base</strong> <strong>function</strong> to coordinate these factors<br />
within the craniofacial complex during<br />
growth <strong>and</strong> development? As noted above,<br />
these questions need to be addressed using
160 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
two approaches. Ontogenetic studies are<br />
crucial for testing hypotheses about the generation<br />
of morphological covariation patterns,<br />
<strong>and</strong> comparative studies are important<br />
for probing the extent to which<br />
interspecific patterns of morphological evolution<br />
are epiphenomena of developmental<br />
processes.<br />
What major factors generate variation<br />
in the <strong>cranial</strong> <strong>base</strong>?<br />
<strong>The</strong> studies summarized above suggest<br />
that relative brain size, particularly relative<br />
to basi<strong>cranial</strong> length, is an important determinant<br />
of the degree of basi<strong>cranial</strong> angulation.<br />
However, the effects of (especially<br />
prenatal) brain shape on basi<strong>cranial</strong><br />
morphology have yet to be thoroughly investigated.<br />
Further experimental <strong>and</strong> comparative<br />
morphological research is needed to<br />
relate soft-tissue <strong>and</strong> bony morphology in<br />
the <strong>primate</strong> head. Despite a long tradition<br />
suggesting links between basi<strong>cranial</strong> morphology<br />
<strong>and</strong> head, neck, or body posture,<br />
there is currently little empirical support<br />
for the hypothesis that these factors are directly<br />
related to variation in the <strong>cranial</strong><br />
<strong>base</strong>, especially angulation in the midsagittal<br />
plane. Better data are also needed on<br />
head <strong>and</strong> neck posture during locomotion<br />
before locomotor-related <strong>cranial</strong> adaptations<br />
can be definitively identified. However,<br />
connections between facial orientation<br />
<strong>and</strong> basi<strong>cranial</strong> morphology on the one h<strong>and</strong><br />
<strong>and</strong> head posture on the other leave open<br />
the possibility of an indirect link between<br />
basi<strong>cranial</strong> angle <strong>and</strong> head posture.<br />
What role does the <strong>cranial</strong> <strong>base</strong> play in<br />
craniofacial integration?<br />
Because many variables influence <strong>cranial</strong><br />
<strong>base</strong> shape, it follows that these variables<br />
also influence other aspects of <strong>cranial</strong> shape<br />
via the <strong>cranial</strong> <strong>base</strong>. Consequently, a key<br />
issue that emerges repeatedly in discussions<br />
of the role of the basicranium in <strong>cranial</strong><br />
development, growth, <strong>and</strong> evolution is<br />
integration. Integration, which is defined<br />
here as “the association of elements through<br />
a set of causal mechanisms so that change<br />
in one element is reflected by change in<br />
another” (Smith, 1996, p. 70), thereby generating<br />
a pattern of significant covariation<br />
(see also Olson <strong>and</strong> Miller, 1958; Cheverud,<br />
1982; Zelditch, 1988), 11 is an important issue<br />
because of the many genetic, developmental,<br />
<strong>and</strong> <strong>function</strong>al interactions that occur<br />
between the basicranium <strong>and</strong> its<br />
neighboring anatomical components. As described<br />
above, the <strong>cranial</strong> <strong>base</strong> is likely to<br />
directly interact, developmentally <strong>and</strong> <strong>function</strong>ally,<br />
with various adjoining skeletal,<br />
muscular, <strong>and</strong> neurosensory complexes,<br />
most notably the brain, the orbits, the ethmomaxillary<br />
complex, <strong>and</strong> the neck. <strong>The</strong>se<br />
“units,” in turn, have direct <strong>and</strong> indirect<br />
interactions with other putative units such<br />
as the oropharynx, nasopharynx, m<strong>and</strong>ible,<br />
<strong>and</strong> maxillary arches.<br />
But does the <strong>cranial</strong> <strong>base</strong> play an active or<br />
a passive role in integrating <strong>cranial</strong> shape<br />
among these disparate units, <strong>and</strong> how much<br />
integration actually occurs? On an intuitive<br />
level, there are several reasons to suggest<br />
that the <strong>cranial</strong> <strong>base</strong> acts in part as a structural<br />
“interface” during growth between the<br />
brain <strong>and</strong> the face, <strong>and</strong> between the head<br />
<strong>and</strong> the neck. In many regions, the basicranium<br />
serves as the actual structural boundary<br />
between disparate components of the<br />
skull: the floor of the anterior <strong>cranial</strong> fossa<br />
is the roof of the orbits; the back of the<br />
midface is the front of the middle <strong>cranial</strong><br />
fossa; <strong>and</strong> the posterior <strong>cranial</strong> <strong>base</strong> is the<br />
posterior roof of the oropharynx. Yet, in<br />
spite of these obvious relationships, it is<br />
difficult to define or assess quantitative hypotheses<br />
about craniofacial integration because<br />
we know so little about the extent <strong>and</strong><br />
nature of the numerous interactions that<br />
presumably occur between <strong>and</strong> among regions<br />
of the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> other parts of<br />
the skull. What are the actual units in the<br />
<strong>cranial</strong> <strong>base</strong> <strong>and</strong> skull that interact, <strong>and</strong><br />
what regulates their interrelations <strong>and</strong>, especially,<br />
interactions? In other words, the<br />
appropriate null hypothesis to be tested is<br />
that the <strong>cranial</strong> <strong>base</strong>, while associated with<br />
variation in other parts of the skull, plays<br />
11 Note that some researchers (most notably Olson <strong>and</strong> Miller,<br />
1958) define morphological integration solely as a multivariate<br />
pattern of covariation with regard to some a priori biological<br />
hypothesis (thus recognizing the importance of generative processes),<br />
whereas others (e.g., Cheverud, 1996) define integration<br />
more generally as either a pattern or a process that refers to<br />
“connections or relationships among morphological elements.”
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 161<br />
no more of an integrative role than any<br />
other part of the skull (e.g., the m<strong>and</strong>ible,<br />
the brain).<br />
In order to explore the basicranium’s role<br />
in craniofacial integration, it is first necessary<br />
to decide how to test hypotheses about<br />
the many different processes through which<br />
integration occurs, <strong>and</strong> the many structural<br />
<strong>and</strong> <strong>function</strong>al levels at which integration is<br />
evident. Readers interested in this huge <strong>and</strong><br />
complex topic (which is too large to review<br />
thoroughly here) should consult the recent<br />
review by Chernoff <strong>and</strong> Magwene (1999). As<br />
a first-order analysis, it is useful to test<br />
hypotheses about developmental integration<br />
by considering the processes by which<br />
different components of a system influence<br />
one another. Thus, in the context of <strong>cranial</strong><br />
<strong>base</strong> growth within the skull, integration<br />
can occur through the direct inductive<br />
<strong>and</strong>/or mechanical effects of neighboring tissue-tissue<br />
interactions (see Moss, 1997);<br />
through secondary effects of growth in one<br />
region causing changes in the positional relationships<br />
among bones in other regions;<br />
<strong>and</strong> genetically through single genes which<br />
have effects on multiple regions, or through<br />
the coordinated action of multiple genes via<br />
pleiotropy <strong>and</strong> linkage (Atchley <strong>and</strong> Hall,<br />
1991; Cheverud, 1982, 1995, 1996; Zelditch<br />
<strong>and</strong> Fink, 1995, Zelditch <strong>and</strong> Fink, 1996;<br />
Chernoff <strong>and</strong> Magwene, 1999). Of course,<br />
the strength of such ontogenetic interactions<br />
can vary due to changes in the timing<br />
of developmental events, something of great<br />
importance for the analysis of heterochrony,<br />
as well as due to allometric (size-correlated,<br />
size-required) factors. Note that we consider<br />
here integration solely in terms of developmental<br />
events <strong>and</strong> processes (e.g., epigenetic<br />
responses to mechanical loading, displacement<br />
due to cell division), but it is<br />
useful to recognize that developmental integration<br />
leads to, <strong>and</strong> is sometimes caused<br />
by, structural <strong>and</strong> <strong>function</strong>al integration.<br />
Another problem with assessing any integrative<br />
role of the <strong>cranial</strong> <strong>base</strong> within the<br />
skull is the lack of widely accepted criteria<br />
for testing hypotheses of integration. Following<br />
Olson <strong>and</strong> Miller (1958) <strong>and</strong><br />
Chernoff <strong>and</strong> Magwene (1999), we apply<br />
three nonexclusive criteria (correlation, constraint,<br />
<strong>and</strong> ontogenetic sequence) in a preliminary<br />
fashion to solely phenotypic variation<br />
in the <strong>cranial</strong> <strong>base</strong>, using the data<br />
presented above.<br />
Correlation. Integration is most basically<br />
revealed by complex patterns of correlation<br />
<strong>and</strong> covariation which indicate a lack<br />
of independence among variables (see Cheverud,<br />
1995, 1996), <strong>and</strong> which can be recognized<br />
a posteriori by comparing theoretically<br />
<strong>and</strong> empirically derived correlation<br />
matrices (Cheverud, 1982; Shea, 1985b;<br />
Zelditch, 1987, 1988; Cheverud et al., 1989;<br />
Wagner, 1989). Such studies have yet to be<br />
carried out for models that explicitly focus<br />
on the <strong>primate</strong> <strong>cranial</strong> <strong>base</strong> (but see Cheverud,<br />
1995). However, as noted above, a<br />
high degree of covariation is frequently evident<br />
in interspecific analyses of variation<br />
in the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> other parts of the<br />
skull. Perhaps the most obvious example of<br />
this phenomenon is the percentage of variation<br />
in <strong>cranial</strong> <strong>base</strong> angle accounted for by<br />
factors such as brain volume, basi<strong>cranial</strong><br />
length, facial angle, <strong>and</strong> posture. IRE1,<br />
which appears to be the dominant factor<br />
that influences <strong>cranial</strong> <strong>base</strong> angle in <strong>primate</strong>s,<br />
explains 58% of the variation in<br />
CBA1 <strong>and</strong> 38% of the variation in CBA4 (see<br />
Table 5). Furthermore, according to Ross<br />
<strong>and</strong> Ravosa (1993, their Table 2), orbital<br />
axis orientation explains 41% of the variation<br />
in CBA4 among <strong>primate</strong>s, while facial<br />
orientation explains 22% of the variation in<br />
CBA4 among <strong>primate</strong>s. <strong>The</strong> partial correlation<br />
analysis of Strait <strong>and</strong> Ross (1999) (discussed<br />
above) found that IRE explained 36%<br />
of the variation in CBA1 when the effects of<br />
orbital axis <strong>and</strong> head-neck angle were factored<br />
out. Further evidence for this sort of<br />
complex pattern of covariation is documented<br />
among humans between CBA, <strong>cranial</strong><br />
<strong>base</strong> length, <strong>cranial</strong> <strong>base</strong> width, <strong>and</strong><br />
brain volume (Lieberman et al., 2000).<br />
<strong>The</strong>se results are indicative (but not proof)<br />
of a pattern whereby multiple factors combine<br />
to influence CBA in such a way that<br />
variation in CBA itself may play some role<br />
in modulating the interactions among different,<br />
spatially separated components of<br />
the cranium. This hypothesis, however, requires<br />
further testing with comparative ontogenetic<br />
data.
162 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Constraint. Another expected outcome of<br />
integration is constraint, which is defined<br />
most generally as a restriction or limitation<br />
on variation. Regardless of their causes,<br />
which can be phylogenetic, <strong>function</strong>al, developmental,<br />
or structural (Alberch, 1985;<br />
Maynard Smith et al., 1985), constraints are<br />
most basically evident in patterns of invariance.<br />
<strong>The</strong>re has not been much work on<br />
phenotypic constraint in the <strong>cranial</strong> <strong>base</strong>,<br />
but several examples suggest it deserves<br />
further research. One source of evidence for<br />
constraint is revealed by allometry, which<br />
measures size-related conservation of shape<br />
(keeping in mind that size-correlated patterns<br />
due to epigenetic <strong>and</strong> perhaps genetic<br />
factors differ from size-required patterns<br />
that have a primarily <strong>function</strong>al basis). As<br />
Table 4 (see also Strait, 1999; McCarthy,<br />
2001) illustrates, there are numerous,<br />
strongly correlated ontogenetic scaling relationships<br />
across <strong>primate</strong>s between various<br />
components of the <strong>cranial</strong> <strong>base</strong>, the volume<br />
of neural regions, <strong>and</strong> facial dimensions. Integration<br />
between the brain <strong>and</strong> face via the<br />
<strong>cranial</strong> <strong>base</strong> is implied by the fact that many<br />
scaling relationships between contiguous<br />
anatomical units (e.g., the noncortical brain<br />
<strong>and</strong> the posterior <strong>cranial</strong> <strong>base</strong>) result in additional<br />
strongly correlated scaling relationships<br />
between noncontiguous anatomical<br />
units, such as those between brain volume<br />
<strong>and</strong> facial size. <strong>The</strong>se scaling relationships<br />
require more study.<br />
Another potential source of evidence regarding<br />
the presence of a constraint are patterns<br />
of angular invariance. One important<br />
example is the apparently invariant 90° angle<br />
between the PM plane <strong>and</strong> the NHA,<br />
<strong>and</strong> the limited variability that results from<br />
this relationship on the angle between the<br />
PM plane <strong>and</strong> both the planum sphenoideum<br />
<strong>and</strong> the anterior <strong>cranial</strong> <strong>base</strong> (S-FC)<br />
in anthropoids (McCarthy <strong>and</strong> Lieberman,<br />
2001). Other less secure examples of invariance<br />
may include the relationship between<br />
cribriform plate orientation <strong>and</strong> facial orientation<br />
(Ravosa <strong>and</strong> Shea, 1994), <strong>and</strong> the<br />
near 45° angle between the external auditory<br />
meatus, the maxillary tuberosities, <strong>and</strong><br />
the midpoint of the orbital aperture (Bromage,<br />
1992). Further research, however, is<br />
needed on the extent to which invariant angles<br />
<strong>and</strong> spatial relationships occur in the<br />
skull, <strong>and</strong> additional research is needed to<br />
assess the developmental, structural, <strong>and</strong><br />
<strong>function</strong>al <strong>base</strong>s of these relationships, <strong>and</strong><br />
whether they reflect constraints that result<br />
from integration.<br />
Ontogenetic sequence. Finally, hypotheses<br />
of phenotypic integration may sometimes<br />
be inferred or tested by examining<br />
ontogenetic sequences during normal<br />
growth <strong>and</strong> in the context of controlled experiments.<br />
Ontogenetic data allow one to<br />
test hypotheses of integration by examining<br />
the structural relationships between one<br />
variable <strong>and</strong> another during growth (e.g.,<br />
heterochrony, heterotopy), <strong>and</strong> to compare<br />
the pattern <strong>and</strong> timing of developmental<br />
events. So far, there have been few attempts<br />
to examine hypotheses of integration in the<br />
<strong>cranial</strong> <strong>base</strong> using ontogenetic data (especially<br />
from embryonic stages), but a few examples<br />
indicate that the sequence of interactions<br />
between the <strong>cranial</strong> <strong>base</strong>, the face,<br />
<strong>and</strong> the brain are complex <strong>and</strong> multiphasic,<br />
with the <strong>cranial</strong> <strong>base</strong> mediating various interactions<br />
between the face <strong>and</strong> the brain.<br />
For example, the prenatal human <strong>cranial</strong><br />
<strong>base</strong> initially flexes, then remains stable,<br />
<strong>and</strong> then extends, all during periods of rapid<br />
neural growth (Jeffery, 1999). Postnatally,<br />
the nonhuman <strong>primate</strong> <strong>cranial</strong> <strong>base</strong> (best<br />
studied in Pan <strong>and</strong> Macaca) appears to extend<br />
slightly during the period of neural<br />
growth, <strong>and</strong> subsequently extends more<br />
rapidly <strong>and</strong> for a long time as the face continues<br />
to grow. In contrast, the human <strong>cranial</strong><br />
<strong>base</strong> flexes rapidly during the first few<br />
years of brain growth, <strong>and</strong> subsequently remains<br />
stable. <strong>The</strong>se contrasting sequences<br />
imply multiple interactions between the<br />
brain <strong>and</strong> the face via the <strong>cranial</strong> <strong>base</strong>, but<br />
have yet to be resolved in terms of the actual<br />
processes that cause flexion <strong>and</strong> extension<br />
at specific locations during different periods<br />
of growth. One hypothesis, which remains<br />
to be tested, is that the <strong>cranial</strong> <strong>base</strong> <strong>function</strong>s<br />
to accommodate <strong>and</strong> perhaps coordinate<br />
these different aspects of growth. Controlled<br />
experimental studies, which can<br />
potentially isolate local <strong>and</strong> regional effects<br />
of specific growth stimuli on the <strong>cranial</strong> <strong>base</strong><br />
<strong>and</strong> the rest of the skull, are a promising
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 163<br />
avenue for future research on this problem<br />
(see Sarnat, 1982; Bütow, 1990; Reidenberg<br />
<strong>and</strong> Laitman, 1991).<br />
Future research<br />
Although the <strong>cranial</strong> <strong>base</strong> does appear to<br />
play some integrative role in the cranium,<br />
we have only a vague, incomplete picture of<br />
how this integration occurs, <strong>and</strong> how much<br />
of a role it plays in influencing various aspects<br />
of craniofacial form <strong>and</strong> <strong>function</strong>, <strong>and</strong><br />
how these processes relate to evolutionary<br />
shifts in the <strong>primate</strong> <strong>cranial</strong> <strong>base</strong>. More research<br />
is needed to isolate <strong>and</strong> define the<br />
actual morphogenetic units which interact,<br />
to identify <strong>and</strong> quantify their direct <strong>and</strong> indirect<br />
interactions, <strong>and</strong> to underst<strong>and</strong> the<br />
processes by which they interact. <strong>The</strong>se<br />
goals may be accomplished by combining at<br />
least four approaches. First, we need to<br />
gather more three-dimensional data on <strong>cranial</strong><br />
<strong>base</strong> variation in ontogenetic samples<br />
at all stages of growth <strong>and</strong> development (fetal<br />
to adult) among different species. <strong>The</strong><br />
<strong>cranial</strong> <strong>base</strong> <strong>and</strong> the rest of the skull comprise<br />
a complex three-dimensional structure<br />
whose internal <strong>and</strong> external structures differ<br />
substantially, yet most studies of <strong>cranial</strong><br />
<strong>base</strong> variation so far have used external<br />
l<strong>and</strong>marks <strong>and</strong>/or two-dimensional radiographic<br />
analysis of midsagittal l<strong>and</strong>marks<br />
(or nonmidsagittal l<strong>and</strong>marks projected into<br />
the midsagittal plane). Second, more data<br />
are needed on the developmental mechanisms<br />
which generate variation in the <strong>cranial</strong><br />
<strong>base</strong>, <strong>and</strong> which regulate interactions<br />
among components of the skull. Experimental,<br />
histological, <strong>and</strong> other kinds of developmental<br />
information will be useful in this<br />
regard, because observed morphological<br />
patterns are potentially generated by different<br />
genetic <strong>and</strong> epigenetic processes. Third,<br />
more data are needed on the genetic <strong>base</strong>s<br />
for variation in <strong>cranial</strong> <strong>base</strong> growth <strong>and</strong><br />
form. Lastly, more detailed interspecific<br />
analyses are needed to extend the evolutionary<br />
implications of ontogenetic tests of hypotheses<br />
about interactions <strong>and</strong> relationships<br />
among morphogenetic units of the<br />
skull. Such future research on the <strong>cranial</strong><br />
<strong>base</strong> should provide interesting <strong>and</strong> valuable<br />
insights on other aspects of craniofacial<br />
growth, <strong>function</strong>, <strong>and</strong> evolution in <strong>primate</strong>s<br />
<strong>and</strong> other mammals.<br />
ACKNOWLEDGMENTS<br />
We thank N. Jeffery, W. Jungers, R. Mc-<br />
Carthy, C. Ruff, B. Shea, F. Spoor, <strong>and</strong> two<br />
anonymous reviewers for their comments<br />
<strong>and</strong> assistance.<br />
LITERATURE CITED<br />
Adams LM, Moore WJ. 1975. A biomechanical appraisal<br />
of some skeletal features associated with head balance<br />
<strong>and</strong> posture in the Hominoidea. Acta Anat<br />
(Basel) 92:580–594.<br />
Aiello L, Dean C. 1990. An introduction to human evolutionary<br />
anatomy. San Diego: Academic Press.<br />
Alberch P. 1985. Developmental constraints: why St.<br />
Bernards often have an extra digit <strong>and</strong> poodles never<br />
do. Am Nat 126:430–433.<br />
Allman J. 1977. Evolution of the visual system in early<br />
<strong>primate</strong>s. In: Sprague JM, Epstein JM, editors.<br />
Progress in psychobiology, physiology, <strong>and</strong> psychology.<br />
Volume 7. New York: Academic Press. p 1–53.<br />
Allman J. 1982. Reconstructing the evolution of the<br />
brain in <strong>primate</strong>s through the use of comparative<br />
neurophysiological <strong>and</strong> neuroanatomical data. In:<br />
Armstrong E, Falk D, editors. Primate brain evolution.<br />
New York: Plenum Press. p 13–28.<br />
Allman JM, Kaas JH. 1974. <strong>The</strong> organization of the<br />
second visual area (V II) in the owl monkey: a second<br />
order transformation of the visual hemifield. Brain<br />
Res 76:247–265.<br />
Anagastopolou S, Karamaliki DD, Spyropoulos MN.<br />
1988. Observations on the growth <strong>and</strong> orientation of<br />
the anterior <strong>cranial</strong> <strong>base</strong> in the human foetus. Eur<br />
J Orthod 10:143–148.<br />
Angst R. 1967. Beitrag zum formw<strong>and</strong>el des craniums<br />
der ponginen. Z Morphol Anthropol 58:109–151.<br />
Antón SC. 1989. Intentional <strong>cranial</strong> vault deformation<br />
<strong>and</strong> induced changes in the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> face.<br />
Am J Phys Anthropol 79:253–267.<br />
Antón SC. 1994. Mechanical <strong>and</strong> other perspectives on<br />
Ne<strong>and</strong>ertal craniofacial morphology. In: Corruccini<br />
RS, Ciochon RL, editors. Integrative paths to the<br />
past: palaeoanthropological advances in honor of F.<br />
Clark Howell. Englewood Cliffs, NJ: Prentice Hall. p<br />
677–695.<br />
Ashton EH. 1952. Age changes in the basi<strong>cranial</strong> axis of<br />
the anthropoidea. Proc Zool Soc Lond [Biol] 129:61–<br />
74.<br />
Ashton EH, Spence TF. 1958. Age changes in the <strong>cranial</strong><br />
capacity <strong>and</strong> foramen magnum of hominoids.<br />
Proc Zool Soc Lond [Biol] 130:169–181.<br />
Ashton EH, Zuckerman S. 1952. Age changes in the<br />
position of the occipital condyles in the chimpanzee<br />
<strong>and</strong> gorilla. Am J Phys Anthropol 10:277–288.<br />
Ashton EH, Zuckerman S. 1956. Age changes in the<br />
position of the foramen magnum in hominoids. Proc<br />
Zool Soc Lond [Biol] 126:315–325.<br />
Atchley WR, Hall BK. 1991. A model for development<br />
<strong>and</strong> evolution of complex morphological structures.<br />
Biol Rev 66:101–157.<br />
Babler WJ. 1989. Relationship of altered <strong>cranial</strong> suture<br />
growth to the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> midface. In: Persing<br />
JA, Edgerton MT, Jane JA, editors. Scientific foundations<br />
<strong>and</strong> surgical treatment of craniosynostosis. Baltimore:<br />
Williams <strong>and</strong> Wilkins. p 87–95.<br />
Baer T, Gore JC, Gracco LC, Nye PW. 1991. Analysis of<br />
vocal tract shape <strong>and</strong> dimensions using magnetic res-
164 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
onance imaging: vowels. J Acoust Soc Am 90:799–<br />
828.<br />
Barlow HB. 1986. Why have multiple cortical areas?<br />
Vision Res 26:81–90.<br />
Barton RA. 1998. Visual specialization <strong>and</strong> brain evolution<br />
in <strong>primate</strong>s. Proc R Soc Lond [Biol] 265:1933–<br />
1937.<br />
Baume JL. 1957. A biologist looks at the sella point. Eur<br />
Orthod Soc Trans 33:150–159.<br />
Beard KC. 1993. Phylogenetic systematics of the Primatomorpha,<br />
with special reference to Dermoptera.<br />
In: Szalay FS, Novacek MJ, McKenna MC, editors.<br />
Mammal phylogeny: placentals. New York: Springer-<br />
Verlag. p 129–150.<br />
Beckman ME, Jung T-P, Lee S-H, de Jong K, Krishnamurthy<br />
AK, Ahalt SC, Cohen KB, Collins MJ.<br />
1995. Variability in the production of quantal vowels<br />
revisited. J Acoust Soc Am 97:471–489.<br />
Beechey C, Boyd Y, Searle AG. 1998. Brachyrrhine, Br,<br />
a mouse craniofacial mutant maps to distal mouse<br />
chromosome 17 <strong>and</strong> is a c<strong>and</strong>idate model for midline<br />
cleft syndrome. Mouse Genome 95:692–694.<br />
Biegert J. 1957. Der Formw<strong>and</strong>el der Primatenschädels<br />
und seine Beziehungen zur ontogenetischen Entwicklung<br />
und den phylogenetischen. Gegenbaurs Morphol<br />
Jahrb 98:77–199.<br />
Biegert J. 1963. <strong>The</strong> evaluation of characteristics of the<br />
skull, h<strong>and</strong>s <strong>and</strong> feet for <strong>primate</strong> taxonomy. In: Washburn<br />
SL, editor. Classification <strong>and</strong> human evolution.<br />
Chicago: Aldine. p 116–145.<br />
Björk A. 1955. Cranial <strong>base</strong> development. Am J Orthod<br />
41:198–225.<br />
Bolk L. 1909. On the position <strong>and</strong> displacement of the<br />
foramen magnum in the Primates. Verh Akad Wet<br />
Amst 12:362–377.<br />
Bolk L. 1910. On the slope of the foramen magnum in<br />
Primates. Verh Akad Wet Amst 12:525–534.<br />
Bolk L. 1926. Das Problem der Menschwerdung. Jena:<br />
Gustav Fischer.<br />
Bookstein F. 1991. Morphometric tools for l<strong>and</strong>mark<br />
data: geometry <strong>and</strong> biology. New York: John Wiley<br />
<strong>and</strong> Sons.<br />
Bosma JF, editor. 1976. Development of the basicranium.<br />
Bethesda, MD: National Institutes of Health.<br />
Braga J, Crubezy E, Elyaqtine M. 1999. <strong>The</strong> posterior<br />
border of the sphenoid greater wing <strong>and</strong> its phylogenetic<br />
usefulness in human evolution. Am J Phys Anthropol<br />
107:387–399.<br />
Brodie AG. 1941. On the growth pattern of the human<br />
head from the third month to the eighth year of life.<br />
Am J Anat 68:208–262.<br />
Brodie AG. 1953. Late growth changes in the human<br />
face. Angle Orthod 23:146–157.<br />
Bromage TG. 1992. <strong>The</strong> <strong>ontogeny</strong> of Pan troglodytes<br />
craniofacial architectural relationships <strong>and</strong> implications<br />
for early hominids. J Hum Evol 23:235–251.<br />
Butler AB, Hodos W. 1996. Comparative vertebrate<br />
neuroanatomy, evolution <strong>and</strong> adaptation. New York:<br />
Wiley-Liss.<br />
Bütow K-W. 1990. Craniofacial growth disturbance after<br />
skull <strong>base</strong> <strong>and</strong> associated suture synostoses in the<br />
newborn Chacma baboon: a preliminary report. Cleft<br />
Palate J 27:241–252.<br />
Cameron J. 1924. <strong>The</strong> cranio-facial axis of Huxley. Part<br />
I. Embryological considerations. Trans R Soc Can 18:<br />
115–123.<br />
Cameron J. 1927. <strong>The</strong> main angle of <strong>cranial</strong> flexion (the<br />
nasion-pituitary-basion angle). Am J Phys Anthropol<br />
10:275–279.<br />
Cameron J. 1930. Craniometric memoirs. No. II. <strong>The</strong><br />
human <strong>and</strong> comparative anatomy of Cameron’s<br />
craniofacial axis. J Anat 64:324–336.<br />
Carre R, Lindblom B, MacNeilage P. 1994. Acoustic<br />
factors in the evolution of the human vocal tract. J<br />
Acoust Soc Am 95:2924.<br />
Cartmill M. 1970. <strong>The</strong> orbits of arboreal mammals.<br />
Ph.D. dissertation, <strong>University</strong> of Chicago.<br />
Cartmill M. 1972. Arboreal adaptations <strong>and</strong> the origin<br />
of the order Primates. In: Tuttle RH, editor. <strong>The</strong> <strong>function</strong>al<br />
<strong>and</strong> evolutionary biology of <strong>primate</strong>s. Chicago:<br />
Aldine. p 97–122.<br />
Cartmill M. 1974. Rethinking <strong>primate</strong> origins. Science<br />
184:436–443.<br />
Cartmill M. 1980. Morphology, <strong>function</strong>, <strong>and</strong> evolution<br />
of the anthropoid postorbital septum. In: Ciochon RL<br />
Chiarelli AB, editors. Evolutionary biology of the New<br />
World monkeys <strong>and</strong> continental drift. New York: Plenum<br />
Press. p 243–274.<br />
Cartmill M. 1992. New views on <strong>primate</strong> origins. Evol<br />
Anthropol 1:105–111.<br />
Chan L-K. 1991. <strong>The</strong> deduction of the level of the human<br />
larynx from bony l<strong>and</strong>marks: its relevance to the<br />
evolution of speech. Hum Evol 6:249–261.<br />
Cherniak C. 1995. Neural component placement.<br />
Trends Neurosci 18:522–527.<br />
Chernoff B, Magwene P. 1999. Morphological integration:<br />
forty years later. In: Olson EC, Miller RL, editors.<br />
Morphological integration. Chicago: <strong>University</strong><br />
of Chicago Press. p 319–348.<br />
Cheverud JM. 1982. Phenotypic, genetic, <strong>and</strong> environmental<br />
morphological integration in the cranium.<br />
Evolution 36:499–516.<br />
Cheverud JM. 1995. Morphological integration in the<br />
saddle back tamarin (Saguinas fuscicollis) cranium.<br />
Am Nat 145:63–89.<br />
Cheverud JM. 1996. Developmental integration <strong>and</strong> the<br />
evolution of pleiotropy. Am Zool 36:44–50.<br />
Cheverud JM, Buikstra J. 1982. Quantitative genetics<br />
of skeletal non-metric traits in the rhesus macaques<br />
on Cayo Santiago III. Relative heritability of skeletal<br />
metric <strong>and</strong> non-metric traits. Am J Phys Anthropol<br />
59:151–155.<br />
Cheverud JM, Richtsmeier J. 1986. Finite element scaling<br />
applied to sexual dimorphism in rhesus macaque<br />
(Macaca mulatta) facial growth. Syst Zool 35:381–<br />
399.<br />
Cheverud JM, Dow MM, Leutenegger W. 1985. <strong>The</strong><br />
quantitative assessment of phylogenetic constraints<br />
in comparative analyses: sexual dimorphism in body<br />
weight among <strong>primate</strong>s. Evolution 39:1335–1351.<br />
Cheverud JM, Wagner GP, Dow MM. 1989. Methods for<br />
the comparative analysis of variation patterns. Syst<br />
Zool 38:201–213.<br />
Cheverud JM, Kohn LAP, Konigsberg LW, Leigh SR.<br />
1992. <strong>The</strong> effects of fronto-occipital artifical <strong>cranial</strong><br />
vault modification on the <strong>cranial</strong> <strong>base</strong> <strong>and</strong> face. Am J<br />
Phys Anthropol 88:323–345.<br />
Couly GF, Coltey PM, Le Douarin NM. 1993. <strong>The</strong> triple<br />
origin of skull in higher vertebrates. Development<br />
117:409–429.<br />
Cousin RP, Fenart R, Deblock R. 1981. Variations ontogénétiques<br />
des angles basicraniens et faciaux. Bull<br />
Mem Soc Anthropol Paris 8:189–212.<br />
Covert HH, Hamrick MW. 1993. Description of new<br />
skeletal remains of the early Eocene anaptomorphine<br />
<strong>primate</strong> Absarokius (Omomyidae) <strong>and</strong> a discussion<br />
about its adaptive profile. J Hum Evol 25:351–362.<br />
Cramer DL. 1977. Craniofacial morphology of Pan paniscus:<br />
a morphometric <strong>and</strong> evolutionary appraisal.<br />
Contrib Primatol 10:1–64.<br />
Crelin E. 1969. Anatomy of the newborn: an atlas. Philadelphia:<br />
Lea <strong>and</strong> Febiger.<br />
Crelin ES. 1973. Functional anatomy of the newborn:<br />
an atlas. New Haven: Yale <strong>University</strong> Press.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 165<br />
Crompton AW, German RZ, <strong>The</strong>xton AJ. 1997. Mechanisms<br />
of swallowing <strong>and</strong> airway protection in infant<br />
mammals (Sus domesticus <strong>and</strong> Macaca fascicularis).<br />
J Zool Lond 241:89–102.<br />
Dabelow A. 1929. Über Korrelationenin der phylogenetischen<br />
Entwicklung der Schädelform. Gegenbaurs<br />
Morphol Jahrb 63:1–49.<br />
Dabelow A. 1931. Über Korrelationenin der phylogenetischen<br />
Entwicklung der Schädelform. II. Die Beziehungen<br />
zwischen Gehirn und Schädelbasisform bei<br />
den Mammaliern. Gegenbaurs Morphol Jahrb 67:84–<br />
133.<br />
Dagosto M. 1988. Implications of post<strong>cranial</strong> evidence<br />
for the origin of eu<strong>primate</strong>s. J Hum Evol 17:35–56.<br />
David DJ, Hemmy DC, Cooter RD. 1989. Craniofacial<br />
deformities. New York: Springer Verlag.<br />
Dean MC. 1988. Growth processes in the <strong>cranial</strong> <strong>base</strong> of<br />
hominoids <strong>and</strong> their bearing on the morphological<br />
similarities that exist in the <strong>cranial</strong> <strong>base</strong> of Homo <strong>and</strong><br />
Paranthropus. In: Grine FE, editor. Evolutionary history<br />
of the “robust” Australopithecines. New York:<br />
Aldine. p 107–112.<br />
Dean MC, Wood BA. 1981. Metrical analysis of the<br />
basicranium of extant hominoids <strong>and</strong> Australopithecus.<br />
Am J Phys Anthropol 59:53–71.<br />
Dean MC, Wood BA. 1982. Basi<strong>cranial</strong> anatomy of Plio-<br />
Pleistocene hominids from East <strong>and</strong> South Africa.<br />
Am J Phys Anthropol 59:157–174.<br />
de Beer GR. 1937. <strong>The</strong> development of the vertebrate<br />
skull. Oxford: Oxford <strong>University</strong> Press.<br />
Delattre A, Fenart R. 1956. Le développement du crâne<br />
du gorille et du chimpanzé comparé au développement<br />
du crâne humain. Bull Mem Soc Anthropol<br />
Paris 6:159–173.<br />
Delattre A, Fenart R. 1963. Études des projections horizontale<br />
et vertico-frontales du crâne au cours de<br />
l’hominisation. Anthropologie 67:525–561.<br />
Demes AB. 1985. Biomechanics of the <strong>primate</strong> skull<br />
<strong>base</strong>. Advances in anatomy, embryology <strong>and</strong> cell biology.<br />
Volume 94. Berlin: Springer-Verlag.<br />
Diewert VM. 1985. Development of human craniofacial<br />
morphology during the late embryonic <strong>and</strong> early fetal<br />
periods. Am J Orthod 88:64–76.<br />
Dmoch R. 1975. Beiträge zum formenw<strong>and</strong>el des <strong>primate</strong>ncraniums<br />
mit bemerkungen zu den sagittalen<br />
knickungsverhältnissen. II Streckenanalyse, I, Neurocranium.<br />
Gegenbaurs Morphol Jahrb 121:521–601.<br />
DuBrul EL. 1950. Posture, locomotion <strong>and</strong> the skull in<br />
Lagomorpha. Am J Anat 87:277–313.<br />
DuBrul EL. 1977. Early hominid feeding mechanisms.<br />
Am J Phys Anthropol 47:305–320.<br />
DuBrul EL. 1979. Origin <strong>and</strong> adaptations of the hominid<br />
jaw joint. In: Sarnat BG, Laskin DM, editors. <strong>The</strong><br />
temporom<strong>and</strong>ibular jaw joint. 3rd ed. Springfield, IL:<br />
Thomas. p 5–34.<br />
DuBrul EL, Laskin DM. 1961. Preadaptive potentialities<br />
of the mammalian skull: an experiment in growth<br />
<strong>and</strong> form. Am J Anat 109:117–132.<br />
Duckworth WLH. 1904. Studies from the anthropological<br />
laboratory. Cambridge: Cambridge <strong>University</strong><br />
Press.<br />
Duckworth WLH. 1915. Morphology <strong>and</strong> anthropology.<br />
2nd ed. Cambridge: Cambridge <strong>University</strong> Press.<br />
Duterloo HS, Enlow DH. 1970. A comparative study of<br />
<strong>cranial</strong> growth in Homo <strong>and</strong> Macaca. Am J Anat<br />
127:357–368.<br />
Enlow DH. 1976. Postnatal growth <strong>and</strong> development of<br />
the face <strong>and</strong> cranium. In: Cohen B, Kramer IRV,<br />
editors. Scientific foundations of dentistry. London:<br />
Heinemann. p 29–46.<br />
Enlow DH. 1990. Facial growth. 3rd ed. Philadelphia:<br />
Saunders.<br />
Enlow DH, Azuma M. 1975. Functional growth boundaries<br />
in the human <strong>and</strong> mammalian face. In: Bergsma<br />
D, editor. Morphogenesis <strong>and</strong> malformation of face<br />
<strong>and</strong> brain. New York: A.R. Liss. p 217–230.<br />
Enlow DH, Bhatt MK. 1984. Facial morphology variations<br />
associated with head form variations. J Charles<br />
Tweed Found 12:21–23.<br />
Enlow DH, Hans MG. 1996. Essentials of facial growth.<br />
Philadelphia: W.B. Saunders.<br />
Fant G. 1960. Acoustic theory of speech production. <strong>The</strong><br />
Hague: Mouton.<br />
Felsenstein J. 1985. Phylogenies <strong>and</strong> the comparative<br />
method. Am Nat 125:1–15.<br />
Fenart R. 1966. Changements morphologiques de<br />
l’encéphale, chez le rat amputé des membres antérieurs.<br />
J Hirnforsch 8:493–501.<br />
Fenart R, Pellerin C. 1988. <strong>The</strong> vestibular orientation<br />
method: its application in the determination of an<br />
average human skull type. Int J Anthropol 3:223–<br />
239.<br />
Fleagle JG. 1999. Primate adaptation <strong>and</strong> evolution.<br />
2nd ed. New York: Academic Press.<br />
Ford EH. 1956. <strong>The</strong> growth of the foetal skull. J Anat<br />
90:63–72.<br />
Ford EH. 1958. Growth of the human <strong>cranial</strong> <strong>base</strong>. Am J<br />
Orthod 44:498–506.<br />
George SL. 1978. A longitudinal <strong>and</strong> cross-sectional<br />
analysis of the growth of the postnatal <strong>cranial</strong> <strong>base</strong><br />
angle. Am J Phys Anthropol 49:171–178.<br />
German RZ, Crompton AW, McCluskey C, <strong>The</strong>xton AJ.<br />
1996. Coordination between respiration <strong>and</strong> deglutition<br />
in a preterm infant mammal, Sus scrofa. Arch<br />
Oral Biol 41:619–622.<br />
Giles WB, Philips CL, Joondeph DR. 1981. Growth in<br />
the basi<strong>cranial</strong> synchondroses of adolescent Macaca<br />
mullata. Anat Rec 19:259–266.<br />
Gould SJ. 1975. Allometry in <strong>primate</strong>s, with emphasis<br />
on scaling <strong>and</strong> the evolution of the brain. Contrib<br />
Primatol 5:244–292.<br />
Gould SJ. 1977. Ontogeny <strong>and</strong> phylogeny. Cambridge:<br />
Belknap Press.<br />
Graf W. 1988. Motion detection in physical space <strong>and</strong> its<br />
peripheral <strong>and</strong> central representation. Ann NY Acad<br />
Sci 545:154–169.<br />
Graf W, deWaele C, Vidal PP, Wang DH, Evinger C.<br />
1995. <strong>The</strong> orientation of the cervical vertebral column<br />
in unrestrained awake animals. II. Movement strategies.<br />
Brain Behav Evol 45:209–231.<br />
Hall BK, editor. 1994. Homology: the hierarchical basis<br />
of comparative biology. New York: Academic Press.<br />
Hamrick MW. 1998. Functional <strong>and</strong> adaptive significance<br />
of <strong>primate</strong> pads <strong>and</strong> claws: evidence from New<br />
World anthropoids. Am J Phys Anthropol 106:113–<br />
127.<br />
Hamrick MW. 1999. Pattern <strong>and</strong> process in the evolution<br />
of <strong>primate</strong> nails <strong>and</strong> claws. J Hum Evol 37:293–<br />
297.<br />
Heintz N. 1966. Le crâne des anthropomorphes: croissance<br />
relative, variabilité, évolution. Musée Royale de<br />
l’Afrique Centrale-Tervuren. Ann Sci Zool 6:1–122.<br />
Herring SW. 1993. Epigenetic <strong>and</strong> <strong>function</strong>al influences<br />
on skull growth. In: Hanken J, Hall BK, editors. <strong>The</strong><br />
skull. Volume 1. Chicago: <strong>University</strong> of Chicago<br />
Press. p 153–206.<br />
Hofer H. 1960. Studien zum Problem des Gestaltw<strong>and</strong>els<br />
des Schädels der Säugetiere, insbesondere der<br />
Primaten. I. Die medianen Kruemmundgen des<br />
Schädels und ihr Ehrfassung nach L<strong>and</strong>zert. Z Morphol<br />
Anthropol 50:299–316.<br />
Hofer H. 1965. Die morphologische Analyse des<br />
Schädels des Menschen. In: Hereberer G, editor.
166 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Menschliche Abstammungslehre. Stuttgart: G. Fischer.<br />
p 145–226.<br />
Hofer H. 1969. On the evolution of the craniocerebral<br />
topography in <strong>primate</strong>s. Ann NY Acad Sci 162:341–<br />
356.<br />
Hofer H, Spatz W. 1963. Studien zum Problem des<br />
Gestaltw<strong>and</strong>els des Schädels der Säugetiere, insbesondere<br />
der Primaten. II. Über die kyphosen fetaler<br />
und neonater Primatenschädel. Z Morphol Anthropol<br />
53:29–52.<br />
Hooton EA. 1946. Up from the ape. 3rd ed. New York:<br />
Macmillan.<br />
Howells WW. 1973. Cranial variation in man. Cambridge:<br />
Peabody Museum Papers, no. 67.<br />
Hoyte DA. 1991. <strong>The</strong> <strong>cranial</strong> <strong>base</strong> in normal <strong>and</strong> abnormal<br />
growth. Neurosurg Clin North Am 2:515–537.<br />
Huxley TH. 1867. On two widely contrasted forms of the<br />
human cranium. J Anat Physiol 1:60–77.<br />
Hyl<strong>and</strong>er WL, Ravosa MJ. 1992. An analysis of the<br />
supraorbital region of <strong>primate</strong>s: a morphometric <strong>and</strong><br />
experimental approach. In: Smith P, Tchernov E, editors.<br />
Structure, <strong>function</strong> <strong>and</strong> evolution of teeth. London:<br />
Freund. p 223–255.<br />
Hyl<strong>and</strong>er WL, Ravosa MJ, Ross CF, Johnson KR. 1998.<br />
M<strong>and</strong>ibular corpus strain in <strong>primate</strong>s: further evidence<br />
for a <strong>function</strong>al link between symphyseal fusion<br />
<strong>and</strong> jaw-adductor muscle force. Am J Phys Anthropol<br />
107:257–271.<br />
Hyl<strong>and</strong>er WL, Ravosa MJ, Ross CF, Wall CE, Johnson<br />
KR. 2000. Symphyseal fusion <strong>and</strong> jaw-adductor muscle<br />
force: an EMG study. Am J Phys Anthropol 112:<br />
469–492.<br />
Jeffery N. 1999. Fetal development <strong>and</strong> evolution of the<br />
human <strong>cranial</strong> <strong>base</strong>. Ph.D. dissertation, <strong>University</strong><br />
College, London.<br />
Jerison HJ. 1982. Allometry, brain size <strong>and</strong> convolutedness.<br />
In: Armstrong E, Falk D, editors. Primate brain<br />
evolution. Methods <strong>and</strong> concepts. New York: Plenum<br />
Press. p 77–84.<br />
Jolicoeur P, Mossiman J. 1968. Intervalles de confidance<br />
pour la peute de l’axe majeur d’une distribution<br />
normale bidimensionelle. Biometrie Praximetrie<br />
9:121–140.<br />
K<strong>and</strong>el ER, Schwartz JH, Jessell TM. 1991. Principles<br />
of neural science. 3rd ed. Norwalk, CT: Apple <strong>and</strong><br />
Lang.<br />
Kay RF, Cartmill M. 1974. Skull of Palaechthon nacimienti.<br />
Nature 252:37–38.<br />
Kay RF, Cartmill M. 1977. Cranial morphology <strong>and</strong><br />
adaptations of Palaechthon nacimienti <strong>and</strong> other<br />
Paromomyidae (Plesiadapoidea, ?Primates), with a<br />
description of a new genus <strong>and</strong> species. J Hum Evol<br />
6:19–35.<br />
Kjaer I. 1990. Ossification of the human basicranium. J<br />
Craniofac Genet Dev Biol 10:29–38.<br />
Kodama G. 1976a. Developmental studies of the presphenoid<br />
of the human sphenoid bone. In: Bosma JF,<br />
editor. Development of the basicranium. Bethesda,<br />
MD: National Institutes of Health. p 141–155.<br />
Kodama G. 1976b. Developmental studies of the body of<br />
the human sphenoid bone. In: Bosma JF, editor. Development<br />
of the basicranium. Bethesda, MD: National<br />
Institutes of Health. p. 156–165.<br />
Kodama G. 1976c. Developmental studies of the orbitosphenoid<br />
of the human sphenoid bone. In: Bosma JF,<br />
editor. Development of the basicranium. Bethesda,<br />
MD: National Institutes of Health. p 166–176.<br />
Kohn LAP, Leigh SR, Jacobs SC, Cheverud JM. 1993.<br />
Effects of annular <strong>cranial</strong> vault modification on the<br />
<strong>cranial</strong> <strong>base</strong> <strong>and</strong> face. Am J Phys Anthropol 90:147–<br />
168.<br />
Krogman WM. 1969. Growth changes in the skull, face,<br />
jaws <strong>and</strong> teeth of the chimpanzee. In: Bourne GH,<br />
editor. <strong>The</strong> chimpanzee. Volume 1. Basel: S. Karger. p<br />
104–164.<br />
Lager H. 1958. A histological description of the <strong>cranial</strong><br />
<strong>base</strong> in Macaca rhesus. Eur Orthod Soc Trans 34:147–<br />
156.<br />
Laitman JT, Heimbuch RC. 1982. <strong>The</strong> basicranium of<br />
Plio-Pleistocene hominids as an indicator of their upper<br />
respiratory systems. Am J Phys Anthropol 59:<br />
323–343.<br />
Laitman JT, Reidenberg JS. 1993. Specializations of the<br />
human upper respiratory <strong>and</strong> upper digestive systems<br />
as seen through comparative <strong>and</strong> developmental<br />
anatomy. Dysphagia 8:318–325.<br />
Laitman JT, Heimbuch RC, Crelin ES. 1978. Developmental<br />
change in a basi<strong>cranial</strong> line <strong>and</strong> its relationship<br />
to the upper respiratory system in living <strong>primate</strong>s.<br />
Am J Anat 152:467–483.<br />
Laitman JT, Heimbuch RC, Crelin ES. 1979. <strong>The</strong> basicranium<br />
of fossil hominids as an indicator of their<br />
upper respiratory systems. Am J Phys Anthropol 51:<br />
15–34.<br />
L<strong>and</strong>zert T. 1866. Der Sattelwinkel und sein Verhaeltnis<br />
zur Pro- und Orthognathie. Abh Senckenberg<br />
Naturforsch Ges 6:19–165.<br />
Langille RM, Hall BK. 1993. Pattern formation <strong>and</strong> the<br />
neural crest. In: Hanken J, Hall BK, editors. <strong>The</strong><br />
skull. Volume 1. Chicago: <strong>University</strong> of Chicago<br />
Press. p 77–111.<br />
Larson JE, Herring SW. 1996. Movement of the epiglottis<br />
in mammals. Am J Phys Anthropol 100:71–82.<br />
Latham RA. 1972. <strong>The</strong> sella point <strong>and</strong> postnatal growth<br />
of the human <strong>cranial</strong> <strong>base</strong>. Am J Orthod 61:156–162.<br />
Le Douarin NM, Ziller C, Couly GF. 1993. Patterning of<br />
neural crest derivatives in the avian embryo: in vivo<br />
<strong>and</strong> in vitro studies. Dev Biol 159:24–49.<br />
Lele S. 1993. Euclidean distance matrix analysis<br />
(EDMA): estimation of mean form <strong>and</strong> mean form<br />
difference. Math Geol 25:573–602.<br />
Lemelin P. 1999. Morphological correlates of substrate<br />
use in didelphid marsupials: implications for <strong>primate</strong><br />
origins. J Zool Lond 247:165–175.<br />
Lieberman DE. 1995. Testing hypotheses about recent<br />
human evolution using skulls: integrating morphology,<br />
<strong>function</strong>, development, <strong>and</strong> phylogeny. Curr Anthropol<br />
36:159–197.<br />
Lieberman DE. 1997. Making behavioral <strong>and</strong> phylogenetic<br />
inferences from fossils: considering the developmental<br />
influence of mechanical forces. Annu Rev Anthropol<br />
26:185–210.<br />
Lieberman DE. 1998. Sphenoid shortening <strong>and</strong> the evolution<br />
of modern human <strong>cranial</strong> shape. Nature 393:<br />
158–162.<br />
Lieberman DE. 1999. Homology <strong>and</strong> hominid phylogeny:<br />
problems <strong>and</strong> potential solution. Evol Anthropol<br />
7:142–151.<br />
Lieberman DE. 2000. Ontogeny, homology, <strong>and</strong> phylogeny<br />
in the hominid craniofacial skeleton: the problem<br />
of the browridge. In: O’Higgins P, Cohn M, editors.<br />
Development, growth <strong>and</strong> evolution: implications for<br />
the study of hominid skeletal evolution. London: Academic<br />
Press. p 85–122.<br />
Lieberman DE, McCarthy RC. 1999. <strong>The</strong> <strong>ontogeny</strong> of<br />
<strong>cranial</strong> <strong>base</strong> angulation in humans <strong>and</strong> chimpanzees<br />
<strong>and</strong> its implications for reconstructing pharyngeal<br />
dimensions. J Hum Evol 36:487–517.<br />
Lieberman DE, Pilbeam DR, Wood BA. 1996. Homoplasy<br />
<strong>and</strong> early Homo: an analysis of the evolutionary<br />
relationships of H. habilis sensu stricto <strong>and</strong><br />
H. rudolfensis. J Hum Evol 30:97–120.
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 167<br />
Lieberman DE, McCarthy RC, Hiiemae K, Lieberman<br />
P, Palmer JB. 1998. New estimates of fossil hominid<br />
vocal tract dimension. J Hum Evol 34:12–13.<br />
Lieberman DE, Pearson OM, Mowbray KM. 2000. Basi<strong>cranial</strong><br />
influence on overall <strong>cranial</strong> shape. J Hum<br />
Evol 38:291–315.<br />
Lieberman P. 1984. <strong>The</strong> biology <strong>and</strong> evolution of language.<br />
Cambridge, MA: <strong>Harvard</strong> <strong>University</strong> Press.<br />
Lieberman P, Crelin ES. 1971. On the speech of Ne<strong>and</strong>erthal<br />
man. Ling Inq 1:203–223.<br />
Lieberman P, Crelin ES, Klatt DH. 1972. Phonetic ability<br />
<strong>and</strong> related anatomy of the newborn <strong>and</strong> adult<br />
human, Ne<strong>and</strong>erthal man, <strong>and</strong> the chimpanzee. Am<br />
Anthropol 74:287–307.<br />
Lieberman P, Laitman JT, Reidenberg JS, Gannon PJ.<br />
1992. <strong>The</strong> anatomy, physiology, acoustics <strong>and</strong> perception<br />
of speech: essential elements in analysis of the<br />
evolution of human speech. J Hum Evol 23:447–467.<br />
Lozanoff S. 1993. Midfacial retrusion in adult Brachyrrhine<br />
mice. Acta Anat (Basel) 147:125–132.<br />
Lozanoff S, Jureczek S, Feng T, Padwal R. 1994. Anterior<br />
<strong>cranial</strong> <strong>base</strong> morphology in mice with midfacial<br />
retrusion. Cleft Palate Craniofac J 31:417–428.<br />
Lufkin T, Mark M, Hart CP, Dollé P, LeMeur M, Chambon<br />
P. 1992. Homeotic transformation of the occipital<br />
bones by ectopic expression of a homeobox gene. Nature<br />
359:835–841.<br />
Lugoba SA, Wood BA. 1990. Position <strong>and</strong> orientation of<br />
the foramen magnum in higher <strong>primate</strong>s. Am J Phys<br />
Anthropol 81:67–76.<br />
Ma W, Lozanoff S. 1999. Spatial <strong>and</strong> temporal distribution<br />
of cellular proliferation in the anterior <strong>cranial</strong><br />
<strong>base</strong> of normal midfacially retrusive mice. Clin Anat<br />
12:315–325.<br />
Martin RD. 1990. Primate origins <strong>and</strong> evolution.<br />
Princeton: Princeton <strong>University</strong> Press.<br />
May R, Sheffer DB. 1999. Growth changes in measurements<br />
of upper facial positioning. Am J Phys Anthropol<br />
108:269–280.<br />
Maynard Smith J, Burian R, Kauffman S, Alberch P,<br />
Campbell J, Goodwin B, L<strong>and</strong>e R, Raup D, Wolpert L.<br />
1985. Developmental constraints <strong>and</strong> evolution. Q<br />
Rev Biol 60:265–287.<br />
McCarthy R. 2001. Anthropoid <strong>cranial</strong> <strong>base</strong> architecture<br />
<strong>and</strong> scaling relationships. J Hum Evol (in press).<br />
McCarthy RC, Lieberman DE. 2001. <strong>The</strong> posterior maxillary<br />
(PM) plane <strong>and</strong> anterior <strong>cranial</strong> architecture in<br />
<strong>primate</strong>s. Anat Rec (in press).<br />
Melsen B. 1969. Time of closure of the spheno-occipital<br />
synchondrosis determined on dry skulls. A radiographic<br />
craniometric study. Acta Odontol Sc<strong>and</strong> 27:<br />
73–90.<br />
Melsen B. 1971. <strong>The</strong> postnatal growth of the <strong>cranial</strong><br />
<strong>base</strong> in Macaca rhesus analyzed by the implant<br />
method. T<strong>and</strong>laegebladet 75:1320–1329.<br />
Michejda M. 1971. Ontogenetic changes of the <strong>cranial</strong><br />
<strong>base</strong> in Macaca mulatta. In: Biegert J, Leutenegger<br />
W, editors. Proceedings of the Third International<br />
Congress of Primatology Zurich 1970. Basel: Karger.<br />
p 215–225.<br />
Michejda M. 1972a. <strong>The</strong> role of basi<strong>cranial</strong> synchondroses<br />
in flexure processes <strong>and</strong> ontogenetic development<br />
of the skull <strong>base</strong>. Am J Phys Anthropol 37:143–150.<br />
Michejda M. 1972b. Significance of basi<strong>cranial</strong> synchondroses<br />
in nonhuman <strong>primate</strong>s <strong>and</strong> man. Proc 3rd<br />
Conf Exp Med Surg Primates, Lyon 1:372–378.<br />
Michejda M, Lamey D. 1971. Flexion <strong>and</strong> metric age<br />
changes of the <strong>cranial</strong> <strong>base</strong> in Macaca mulatta. Infants<br />
<strong>and</strong> juveniles. Folia Primatol (Basel) 34:133–<br />
141.<br />
Mitchison G. 1991. Neuronal branching patterns <strong>and</strong><br />
the economy of cortical wiring. Proc R Soc Lond [Biol]<br />
245:151–158.<br />
Moore WJ, Lavelle CJB. 1974. Growth of the facial<br />
skeleton in the Hominoidea. London: Academic Press.<br />
Moore WJ, Adams LM, Lavelle CLB. 1973. Head posture<br />
in the Hominoidea. J Zool Lond 169:409–416.<br />
Moss ML. 1958. <strong>The</strong> pathogenesis of artificial <strong>cranial</strong><br />
deformation. Am J Phys Anthropol 16:269–286.<br />
Moss ML. 1961. Rotation of the otic capsule in bipedal<br />
rats. Am J Phys Anthropol 19:301–307.<br />
Moss ML. 1963. Morphological variations of the crista<br />
galli <strong>and</strong> medial orbital margin. Am J Phys Anthropol<br />
21:259–264.<br />
Moss ML. 1976. Experimental alteration of basi-synchondroseal<br />
cartilage growth in rat <strong>and</strong> mouse. In:<br />
Bosma JF, editor. Development of the basicranium.<br />
Bethesda, MD: National Institutes of Health. p 541–<br />
569.<br />
Moss ML. 1997. <strong>The</strong> <strong>function</strong>al matrix hypothesis revisited.<br />
1. <strong>The</strong> role of mechanotransduction. Am J<br />
Orthod Dentofacial Orthop 112:8–11.<br />
Moss ML, Young RW. 1960. A <strong>function</strong>al approach to<br />
craniology. Am J Phys Anthropol 18:281–292.<br />
Moss ML, Moss-Salentjin L, Vilmann H, Newell-Morris<br />
L. 1982. Neuro-skeletal topology of the <strong>primate</strong> basicranium:<br />
its implications for the “fetalization hypothesis.”<br />
Gegenbaurs Morphol Jahrb 128:58–67.<br />
Nearey T. 1978. Phonetic features for vowels. Bloomington:<br />
Indiana <strong>University</strong> Linguistics Club.<br />
Negus V. 1949. <strong>The</strong> comparative anatomy <strong>and</strong> physiology<br />
of the larynx. New York: Hafner.<br />
Noble VE, Kowalski EM, Ravosa MJ. 2000. Orbital orientation<br />
<strong>and</strong> the <strong>function</strong> of the mammalian postorbital<br />
bar. J Zool Lond 250:405–418.<br />
Noden DM. 1991. Cell movements <strong>and</strong> control of patterned<br />
tissue assembly during craniofacial development.<br />
J Craniofac Genet Dev Biol 11:192–213.<br />
Nunn CL. 1995. A simulation test of Smith’s “degress of<br />
freedom” correction for comparative studies. Am J<br />
Phys Anthropol 98:355–367.<br />
O’Higgins P. 2000. Quantitative approaches to the<br />
study of craniofacial growth <strong>and</strong> evolution: advances<br />
in morphometric techniques. In: O’Higgins P, Cohn<br />
M, editors. Development, growth <strong>and</strong> evolution: implications<br />
for the study of hominid skeletal evolution.<br />
London: Academic Press. p 163–185.<br />
Olson E, Miller R. 1958. Morphological integration. Chicago:<br />
<strong>University</strong> of Chicago Press.<br />
Olson TR. 1985. Cranial morphology <strong>and</strong> systematics of<br />
the Hadar hominids <strong>and</strong> “Australopithecus” africanus.<br />
In: Delson E, editor. Ancestors: the hard evidence.<br />
New York: A.R. Liss. p 102–119.<br />
O’Rahilly R, Müller F. 1999. <strong>The</strong> embryonic human<br />
brain: an atlas of developmental stages. 2nd ed. New<br />
York: Wiley-Liss.<br />
Purvis A, Rambaut A. 1995. Comparative analysis by<br />
independent contrasts (CAIC): an Apple Macintosh<br />
application for analyzing comparative data. Comp<br />
Appl Biosci 11:247–251.<br />
Radinsky LB. 1968. A new approach to mammalian<br />
<strong>cranial</strong> analysis, illustrated by examples of prosimian<br />
<strong>primate</strong>s. J Morphol 124:167–179.<br />
Radinsky LB. 1970. <strong>The</strong> fossil record of prosimian brain<br />
evolution. In: Noback C, Montagna W, editors. <strong>The</strong><br />
<strong>primate</strong> brain. Advances in primatology. Volume 1.<br />
New York: Appleton-Century-Crofts. p 209–224.<br />
Radinsky LB. 1977. Early <strong>primate</strong> brains: facts <strong>and</strong><br />
fiction. J Hum Evol 6:79–86.<br />
Radinsky LB. 1979. <strong>The</strong> fossil evidence of <strong>primate</strong> brain<br />
evolution (James Arthur Lecture). New York: American<br />
Museum of Natural History.
168 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000<br />
Ranke J. 1892. Über einige gesetzmassige Beziehungen<br />
zwischen Schädelgrund, Gehirn- und Gesichtsschädel.<br />
Beitrage Anthropol Urgesch Bayerns 12:1–132.<br />
Ravosa MJ. 1988. Browridge development in Cercopithecidae:<br />
a test of two models. Am J Phys Anthropol<br />
76:535—555.<br />
Ravosa MJ. 1991a. Ontogenetic perspective on mechanical<br />
<strong>and</strong> nonmechanical models of <strong>primate</strong> circumorbital<br />
morphology. Am J Phys Anthropol 85:95–112.<br />
Ravosa MJ. 1991b. Interspecific perspective on mechanical<br />
<strong>and</strong> nonmechanical models of <strong>primate</strong> circumorbital<br />
morphology. Am J Phys Anthropol 86:369–396.<br />
Ravosa MJ. 1996. M<strong>and</strong>ibular form <strong>and</strong> <strong>function</strong> in<br />
North American <strong>and</strong> European Adapidae <strong>and</strong> Omomyidae.<br />
J Morphol 229:171–190.<br />
Ravosa MJ. 1999. Anthropoid origins <strong>and</strong> the modern<br />
symphysis. Folia Primatol (Basel) 70:65–78.<br />
Ravosa MJ, Shea BT. 1994. Pattern in craniofacial biology:<br />
evidence from the Old World monkeys (Cercopithecidae).<br />
Int J Primatol 15:801–822.<br />
Ravosa MJ, Noble VE, Hyl<strong>and</strong>er WL, Johnson KR, Kowalski<br />
EM. 2000a. Masticatory stress, orbital orientation<br />
<strong>and</strong> the evolution of the <strong>primate</strong> postorbital<br />
bar. J Hum Evol 38:667–693.<br />
Ravosa MJ, Vinyard CJ, Hyl<strong>and</strong>er WL. 2000b. Stressed<br />
out: masticatory forces <strong>and</strong> <strong>primate</strong> circumorbital<br />
form. Anat Rec (New Anat) 261:(in press).<br />
Reidenberg JS, Laitman JT. 1991. Effect of basi<strong>cranial</strong><br />
flexion on larynx <strong>and</strong> hyoid position in rats: an experimental<br />
study of skull <strong>and</strong> soft tissue interactions.<br />
Anat Rec 230:557–569.<br />
Riesenfeld A. 1966. <strong>The</strong> effects of experimental bipedalism<br />
<strong>and</strong> upright posture in the rat <strong>and</strong> their significance<br />
for human evolution. Acta Anat (Basel) 65:449–521.<br />
Riesenfeld A. 1969. <strong>The</strong> adaptive m<strong>and</strong>ible: an experimental<br />
study. Acta Anat (Basel) 72:246–262.<br />
Riolo ML, Moyers RE, McNamara JA Jr, Hunter WS.<br />
1974. An atlas of craniofacial growth: cephalometric<br />
st<strong>and</strong>ards from the <strong>University</strong> School Growth Study,<br />
the <strong>University</strong> of Michigan. Ann Arbor: Center for<br />
Human Growth <strong>and</strong> Development, monograph no. 2.<br />
Robinson GW, Mahon KA. 1994. Differential <strong>and</strong> overlapping<br />
expression domains of DLx2 <strong>and</strong> Dlx3 suggest<br />
distinct roles for distal-less genes in craniofacial development.<br />
Mech Dev 48:199–215.<br />
Rosenberger AL. 1985. In favor of the Necrolemur-<br />
Tarsier hypothesis. Folia Primatol (Basel) 45:179–194.<br />
Rosenberger AL. 1986. Platyrrhines, catarrhines <strong>and</strong><br />
the anthropoid transition. In: Wood BA, Martin L,<br />
Andrews P, editors. Major topics in <strong>primate</strong> <strong>and</strong> human<br />
evolution. Cambridge: Cambridge <strong>University</strong><br />
Press. p 66–88.<br />
Ross CF. 1994. Craniofacial evidence for anthropoid <strong>and</strong><br />
tarsier relationships. In: Fleagle JG, Kay RF, editors.<br />
Anthropoid origins. New York: Plenum Press. p 469–<br />
547.<br />
Ross CF. 1995a. Allometric <strong>and</strong> <strong>function</strong>al influences on<br />
<strong>primate</strong> orbit orientation <strong>and</strong> the origins of the Anthropoidea.<br />
J Hum Evol 29:201–227.<br />
Ross CF. 1995b. Muscular <strong>and</strong> osseous anatomy of the<br />
<strong>primate</strong> anterior temporal fossa <strong>and</strong> the <strong>function</strong>s of<br />
the postorbital septum. Am J Phys Anthropol 98:275–<br />
306.<br />
Ross CF. 1996. An adaptive explanation for the origin of<br />
the Anthropoidea (Primates). Am J Primatol 40:205–<br />
230.<br />
Ross CF. 2000. Into the light: the origin of Anthropoidea.<br />
Annu Rev Anthropol 29:147–194.<br />
Ross CF, Henneberg M. 1995. Basi<strong>cranial</strong> flexion, relative<br />
brain size <strong>and</strong> facial kyphosis in Homo sapiens<br />
<strong>and</strong> some fossil hominids. Am J Phys Anthropol 98:<br />
575–593.<br />
Ross CF, Ravosa MJ. 1993. Basi<strong>cranial</strong> flexion, relative<br />
brain size <strong>and</strong> facial kyphosis in nonhuman <strong>primate</strong>s.<br />
Am J Phys Anthropol 91:305–324.<br />
Ross CF, Williams BA, Kay RF. 1998. Phylogenetic<br />
analysis of anthropoid relationships. J Hum Evol 35:<br />
221–306.<br />
Ruff CB, Trinkaus E, Holliday TW. 1997. Body mass<br />
<strong>and</strong> encephalization in Pleistocene Homo. Nature<br />
387:173–176.<br />
Sakka M, Aaron C, Hervé D. 1976. Étude anatomique,<br />
fonctionelle et radiologique de l’ensemble cervicocéphalique<br />
dorsal du Chien. Applications aux problèmes<br />
du port de tête en station érigrée chez les Hominidés.<br />
Zbl Vet Med C 5:1420.<br />
Sarnat BG. 1982. Eye <strong>and</strong> orbital size in the young <strong>and</strong><br />
adult. Some postnatal experimental <strong>and</strong> clinical relationships.<br />
Ophthalmology 185:74–89.<br />
Sarnat BG. 1988. Craniofacial change <strong>and</strong> non-change<br />
after experimental surgery in young <strong>and</strong> adult animals.<br />
Angle Orthod 58:321–342.<br />
Sarnat BG. 1999. Basic science <strong>and</strong> clinical experimental<br />
<strong>primate</strong> studies in craniofaciodental biology: a<br />
personal historical review. J Oral Maxillofac Surg<br />
57:714–724.<br />
Sasaki H, Kodama G. 1976. Developmental studies of<br />
the postsphenoid of the human sphenoid bone. In:<br />
Bosma JF, editor. Development of the basicranium.<br />
Bethesda, MD: National Institutes of Health. p. 177–<br />
190.<br />
Schilling TF, Thorogood PV. 2000. Development <strong>and</strong><br />
evolution of the vertebrate skull. In: O’Higgins P,<br />
Cohn M, editors. Development, growth <strong>and</strong> evolution:<br />
implications for the study of hominid skeletal evolution.<br />
London: Academic Press. p 57–83.<br />
Schneiderman ED. 1992. Facial growth in the rhesus<br />
monkey: a longitudinal <strong>and</strong> cephalometric study.<br />
Princeton: Princeton <strong>University</strong> Press.<br />
Schultz AH. 1940. <strong>The</strong> size of the orbit <strong>and</strong> of the eye in<br />
<strong>primate</strong>s. Am J Phys Anthropol 26:398–408.<br />
Schultz AH. 1942. Conditions for balancing the head in<br />
<strong>primate</strong>s. Am J Phys Anthropol 29:483–497.<br />
Schultz AH. 1955. <strong>The</strong> position of the occipital condyles<br />
<strong>and</strong> of the face relative to the skull <strong>base</strong> in <strong>primate</strong>s.<br />
Am J Phys Anthropol 13:97–120.<br />
Scott JH. 1958. <strong>The</strong> <strong>cranial</strong> <strong>base</strong>. Am J Phys Anthropol<br />
16:319–348.<br />
Shapiro R. 1960. <strong>The</strong> normal skull: a Roentgen study.<br />
New York: Hoeber.<br />
Shapiro R, Robinson F. 1980. <strong>The</strong> embryogenesis of the<br />
human skull. Cambridge: <strong>Harvard</strong> <strong>University</strong> Press.<br />
Shea BT. 1985a. On aspects of skull form in African<br />
apes <strong>and</strong> orangutans, with implications for hominoid<br />
evolution. Am J Phys Anthropol 68:329–342.<br />
Shea BT. 1985b. Ontogenetic allometry <strong>and</strong> scaling: a<br />
discussion <strong>base</strong>d on the growth <strong>and</strong> form of the skull<br />
in African apes. In: Jungers WL, editor. Size <strong>and</strong><br />
scaling in <strong>primate</strong> biology. New York: Plenum Press.<br />
p 175–205.<br />
Shea BT. 1986. On skull form <strong>and</strong> the supraorbital<br />
torus in <strong>primate</strong>s. Curr Anthropol 27:257–259.<br />
Shea BT. 1987. Reproductive strategies, body size, <strong>and</strong><br />
encephalization in <strong>primate</strong> evolution. Int J Primatol<br />
8:139–156.<br />
Shea BT. 1988. Phylogeny <strong>and</strong> skull form in the hominoid<br />
<strong>primate</strong>s. In: Schwartz JH, editor. <strong>The</strong> biology of<br />
the orangutan. New York: Oxford <strong>University</strong> Press. p<br />
233–246.<br />
Simons EL. 1962. Fossil evidence relating to the early<br />
evolution of <strong>primate</strong> behavior. Ann NY Acad Sci 102:<br />
282–294.<br />
Sirianni J. 1985. Nonhuman <strong>primate</strong>s as models for<br />
human craniofacial growth. In: Watt ES, editor. Non-
D.E. Lieberman et al.]<br />
PRIMATE CRANIAL BASE 169<br />
human <strong>primate</strong> models for human growth <strong>and</strong> development.<br />
New York: A.R. Liss. p 95–124.<br />
Sirianni J, Newell-Morris L. 1980. Craniofacial growth<br />
of fetal Macaca nemestrina: a cephalometric roentgenographic<br />
study. Am J Phys Anthropol 53:407–421.<br />
Sirianni JE, Swindler DR. 1979. A review of postnatal<br />
craniofacial growth in Old World monkeys <strong>and</strong> apes.<br />
Yrbk Phys Anthropol 22:80–104.<br />
Sirianni JE, Swindler DR. 1985. Growth <strong>and</strong> development<br />
of the pigtailed macaque. Boca Raton: CRC Press.<br />
Sirianni JE, Van Ness AL. 1978. Postnatal growth of<br />
the <strong>cranial</strong> <strong>base</strong> in Macaca nemestrina. Am J Phys<br />
Anthropol 49:329–340.<br />
Sjøvold T. 1984. A report on the heritability of some<br />
<strong>cranial</strong> measurements <strong>and</strong> non-metric traits. In: Van<br />
Vark GN, Howells WW, editors. Multivariate statistics<br />
in physical anthropology. Dordrecht: D. Reidel. p<br />
223–246.<br />
Slavkin HC. 1989. Developmental craniofacial biology.<br />
Philadelphia: Lea <strong>and</strong> Febiger.<br />
Smith KK. 1996. Integration of craniofacial structures<br />
during development in mammals. Am Zool 26:70–79.<br />
Smith RJ. 1994. Degrees of freedom in interspecific<br />
allometry: an adjustment for the effects of phylogenetic<br />
constraint. Am J Phys Anthropol 93:95–107.<br />
Smith RJ, Josell SD. 1984. <strong>The</strong> plan of the human face: a<br />
test of three general concepts. Am J Orthod 85:103–108.<br />
Sokal RF, Rohlf FJ. 1981. Biometry. 2nd ed. New York:<br />
W.H. Freeman <strong>and</strong> Co.<br />
Sperber GH. 1989. Craniofacial embryology. 4th ed.<br />
London: Wright.<br />
Spoor CF. 1993. <strong>The</strong> comparative morphology <strong>and</strong> phylogeny<br />
of the human bony labyrinth. Ph.D. dissertation,<br />
<strong>University</strong> of Utrecht.<br />
Spoor CF. 1997. Basi<strong>cranial</strong> architecture <strong>and</strong> relative<br />
brain size of Sts 5 (Australopithecus africanus) <strong>and</strong><br />
other Plio-Pleistocene hominids. S Afr J Sci 93:182–186.<br />
Spoor CF, Zonneveld F. 1998. A comparative review of<br />
the human bony labyrinth. Yrbk Phys Anthropol 41:<br />
211–251.<br />
Spoor CF, O’Higgins P, Dean MC, Lieberman DE. 1999.<br />
Anterior sphenoid in modern humans. Nature 397:572.<br />
Spoor CF, Jeffery N, Zonneveld F. 2000. Imaging skeletal<br />
growth <strong>and</strong> evolution. In: O’Higgins P, Cohn M,<br />
editors. Development, growth <strong>and</strong> evolution: implications<br />
for the study of hominid skeletal evolution. London:<br />
Academic Press. p 123–161.<br />
Srivastava HC. 1992. Ossification of the membranous<br />
portion of the squamous part of the occipital bone in<br />
man. J Anat 180:219–224.<br />
Stamrud L. 1959. External <strong>and</strong> internal <strong>cranial</strong> <strong>base</strong>.<br />
Acta Odontol Sc<strong>and</strong> 17:239–266.<br />
Starck D. 1975. <strong>The</strong> skull of the fetal chimpanzee. In:<br />
Bourne GH, editor. <strong>The</strong> chimpanzee. Volume 6. Basel:<br />
S. Karger. p 1–33.<br />
Stephan H, Frahm H, Baron G. 1981. New <strong>and</strong> revised<br />
data on volumes of brain structure in insectivores <strong>and</strong><br />
<strong>primate</strong>s. Comp Primate Biol 4:1–38.<br />
Stevens KN. 1972. Quantal nature of speech. In: David<br />
EE Jr, Denes PB, editors. Human communication: a<br />
unified view. New York: McGraw Hill.<br />
Stevens KN, House AS. 1955. Development of a quantitative<br />
description of vowel articulation. J Acoust Soc<br />
Am 27:484–493.<br />
Strait DS. 1998. Evolutionary integration in the hominid<br />
<strong>cranial</strong> <strong>base</strong>. Ph.D. dissertation, State <strong>University</strong><br />
of New York, Stony Brook.<br />
Strait DS. 1999. <strong>The</strong> scaling of basi<strong>cranial</strong> flexion <strong>and</strong><br />
length. J Hum Evol 37:701–719.<br />
Strait DS, Ross CF. 1999. Kinematic data on <strong>primate</strong><br />
head <strong>and</strong> neck posture: implications for the evolution<br />
of basi<strong>cranial</strong> flexion <strong>and</strong> an evaluation of registration<br />
planes. Am J Phys Anthropol 108:205–222.<br />
Strait DS, Grine FE, Moniz MA. 1997. A reappraisal of<br />
hominid phylogeny. J Hum Evol 32:17–82.<br />
Szalay FS, Rosenberger AL, Dagosto M. 1987. Diagnosis<br />
<strong>and</strong> differentiation of the order Primates. Ybk<br />
Phys Anthropol 30:75–105.<br />
Topinard P. 1890. Anthropology. London: Chapman <strong>and</strong><br />
Hall.<br />
van den Eynde B, Kjaer I, Solo B, Graem N, Kjaer TW,<br />
Mathiesen M. 1992. Cranial <strong>base</strong> angulation <strong>and</strong><br />
prognathism related to <strong>cranial</strong> <strong>and</strong> general skeletal<br />
maturation in human fetuses. J Craniofac Genet Dev<br />
Biol 12:22–32.<br />
Van der Linden FPG, Enlow DH. 1971. A study of the<br />
anterior <strong>cranial</strong> <strong>base</strong>. Am J Orthod 41:119–124.<br />
Van Essen DC. 1997. A tension-<strong>base</strong>d theory of morphogenesis<br />
<strong>and</strong> compact wiring in the central nervous<br />
system. Nature 385:313–318.<br />
Vidal PP, Graf W, Berthoz A. 1986. <strong>The</strong> orientation of the<br />
cervical vertebral column in unrestrained awake animals.<br />
I. Resting position. Exp Brain Res 61:549–559.<br />
Vielle-Grosjean I, Hunt P, Gulisano M, Boncinelli E,<br />
Thorogood PV. 1997. Branchial HOX gene expression<br />
<strong>and</strong> human craniofacial development. Dev Biol 183:<br />
49–60.<br />
Vinyard CI. 1994. A quantitative assessment of the<br />
supraorbital region in moden Melanesians. MA <strong>The</strong>sis<br />
Anthropology, Northern Illinois <strong>University</strong>.<br />
Vinyard CJ, Smith FH. 1997. Morphometric relationships<br />
between the supraorbital region <strong>and</strong> frontal<br />
sinus in Melanesian crania. Homo 48:1–21.<br />
Virchow R. 1857. Untersuchungen über die Entwicklung<br />
des Schädelgrundes im gesunden und<br />
Frankhaften Zust<strong>and</strong>e. Berlin: Gesichissiblung und<br />
Gehirnbru.<br />
Vogel C. 1964. Über eine Schädelbasisanomalie bei<br />
einem freier Wildbahn geschossen Cercopithecus torquatus<br />
atys. Z Morphol Anthropol 55:262–276.<br />
Wagner GP. 1989. <strong>The</strong> biological homology concept.<br />
Annu Rev Ecol Syst 20:51–69.<br />
Weidenreich F. 1941. <strong>The</strong> brain <strong>and</strong> its role in the<br />
phylogenetic transformation of the human skull.<br />
Trans Am Philos Soc 31:321–442.<br />
White TD, Suwa G, Berhane A. 1994. Australopithecus<br />
ramidus, a new species of early hominid from Aramis,<br />
Ethiopia. Nature 371:306–312.<br />
Williams PL, Bannister LH, Berry MM, Collins P,<br />
Dyson M, Dussek JE, Ferguson MWJ. 1995. Gray’s<br />
anatomy. 38th ed. Edinburgh: Churchill Livingstone.<br />
Young RW. 1959. <strong>The</strong> influence of <strong>cranial</strong> contents on<br />
postnatal growth of the skull in the rat. Am J Anat<br />
105:383–390.<br />
Zelditch ML. 1987. Evaluating models of developmental<br />
integration in the laboratory rat using confirmatory<br />
factor analysis. Syst Zool 36:368–380.<br />
Zelditch ML. 1988. Ontogenetic variation in patterns of<br />
phenotypic integration in the laboratory rat. Evolution<br />
42:28–41.<br />
Zelditch ML, Fink WL. 1995. Allometry <strong>and</strong> developmental<br />
integration of body growth in a pirhana, Pygocentrus<br />
natterieri (Teleostei: Ostariophysi). J Morphol<br />
223:341–355.<br />
Zelditch ML, Fink WL. 1996. Heterochrony <strong>and</strong> heterotopy:<br />
stability <strong>and</strong> innovation in the evolution of<br />
form. Paleobiology 22:241–254.<br />
Zuckerman S. 1954. Correlation of change in the evolution<br />
of higher <strong>primate</strong>s. In: Huxley JS, Hardy A, Ford<br />
EB, editors. Evolution as process. London: Allen <strong>and</strong><br />
Unwin. p 347–401.<br />
Zuckerman S. 1955. Age changes in the basi<strong>cranial</strong> axis<br />
of the human skull. Am J Phys Anthropol 13:521–539.