YEARBOOK OF PHYSICAL ANTHROPOLOGY 43:117–169 (2000)

The Primate Cranial Base: Ontogeny, Function, and Integration

DANIEL E. LIEBERMAN,1 CALLUM F. ROSS,2 AND MATTHEW J. RAVOSA3 1Department of Anthropology, George Washington University, Washington, DC 20052, and Human Origins Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560 2Department of Anatomical Sciences, Health Sciences Center, SUNY at Stony Brook, Stony Brook, NY 11794-8081 3Department of Cell and Molecular Biology, Northwestern University Medical School, Chicago, Illinois 60611-3008, and Mammals Division, Department of Zoology, Field Museum of Natural History, Chicago, Illinois 60605-2496 KEY WORDS cranial base; basicranium; chondrocranium; pri- mates; humans

ABSTRACT Understanding the complexities of cranial base develop- ment, function, and architecture is important for testing hypotheses about many aspects of craniofacial variation and evolution. We summarize key aspects of cranial base growth and development in primates that are useful for formulating and testing hypotheses about the roles of the chondrocranium and basicranium in cranial growth, integration, and function in primate and human evolution. We review interspecific, experimental, and ontogenetic evidence for interactions between the cranial base and brain, and between the cranial base and the face. These interactions indicate that the cranial base plays a key role in craniofacial growth, helping to integrate, spatially and functionally, different patterns of growth in various adjoining regions of the skull such as components of the brain, the eyes, the nasal cavity, the oral cavity, and the pharynx. Brain size relative to cranial base length appears to be the dominant influence on many aspects of basicranial variation, espe- cially the angle of the cranial base in the midsagittal plane, but other factors such as facial size, facial orientation, and posture may also be important. Major changes in cranial base shape appear to have played crucial roles in the evolution of early primates, the origin of anthropoids, and the origin of Homo sapiens. Yrbk Phys Anthropol 43:117–169, 2000. © 2000 Wiley-Liss, Inc.

TABLE OF CONTENTS

Glossary, Landmark, and Measurement Definitions ...... 118 Introduction ...... 120 Anatomy and Development ...... 120 Development of the chondrocranium ...... 121 Patterns and processes of basicranial growth ...... 122 Antero-posterior growth ...... 123 Medio-lateral growth ...... 125 Supero-inferior growth ...... 126 Angulation ...... 126 Associations Between Cranial Base and Brain ...... 131 Brain size and cranial base angle ...... 131 Brain shape and cranial base angle ...... 134

© 2000 WILEY-LISS, INC. 118 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 Brain volume and posterior cranial fossa shape ...... 138 Associations Between Cranial Base and Face ...... 138 Anterior cranial fossa shape and upper facial growth ...... 138 Middle cranial fossa shape and midfacial growth ...... 140 Basicranial width and overall facial shape in humans ...... 144 The Cranial Base and Posture ...... 148 Major Unresolved Issues of Cranial Base Variation in Primate Evolution ...... 151 Primate origins, encephalization, and circumorbital form ...... 151 Anthropoid origins and cranial base-face interactions ...... 152 Variation in hominin cranial base angle ...... 153 Cranial base flexion and vocal tract shape in hominins ...... 154 Cranial base shape and facial projection in Homo ...... 156 Cranial base characters in phylogenetic analyses ...... 158 Conclusions ...... 159 What major factors generate variation in the cranial base? ...... 160 What role does the cranial base play in craniofacial integration? ...... 160 Correlation ...... 161 Constraint ...... 162 Ontogenetic sequence ...... 162 Future research ...... 163 Acknowledgments ...... 163 Literature Cited ...... 163

GLOSSARY Drift: a series of events by which an osseous wall “moves” relative to another anatomical Basioccipital clivus: midline “plane” of the posterior cranial base formed by the supe- region through bone deposition on one sur- rior (endocranial) aspects of the basioccipi- face and bone resorption on its opposing tal and the posterior sphenoid. surface. Brain stem: the ventral parts of the brain, Ethmomaxillary complex: the upper part of excluding the telencephalon. Specifically, in the face, mostly comprising the ethmoid, the this paper, the brain stem consists of the nasal capsule, and the maxilla. medulla oblongata and mesencephalon (ϭ Facial projection: degree to which face optic tectum and tegmentum) of Stephan et projects in front of cranial base; measured al. (1981; see also Butler and Hodos, 1996). here by nasion-foramen caecum. Chondrocranium: cartilaginous precursors Integration: the genetic, epigenetic, or func- to the basicranium. tional association among elements via “a set Constraint: a limitation or bias on processes causal mechanisms so that change in one and/or patterns of evolution, growth, form, element is reflected by change in another” and function. (Smith, 1996). The results of integration are Cranial base angulation: a series of events most often recognized as a pattern of signif- by which bone or cartilage deposition in the icant, hierarchical covariation among the midline cranial base changes the angle be- components of a system. tween intersecting prechordal (see below) Kyphosis: angle of some aspect of facial ori- and postchordal (see below) lines. This causes entation relative to the neuro- and/or basi- the inferior cranial base angle to become more cranium, measured here using angle of fa- acute (flexion) or more obtuse (extension). cial kyphosis (AFK) for the orientation of Displacement: a series of events by which the palate, and angle of orbit axis orienta- an osseous region “moves” relative to an- tion (AOA) for orientation of the orbital axis. other osseous region through bone deposi- Planum sphenoideum: midline “plane” of tion (primary displacement), or through the anterior cranial base from the sphenoi- bone deposition in an adjoining bone (sec- dale (Sp) to the planum sphenoideum (PS) ondary displacement). point (see below). D.E. Lieberman et al.] PRIMATE CRANIAL BASE 119 Postchordal cranial base: portion of the cra- ANGLE, LINE, AND PLANE DEFINITIONS nial base posterior to the sella; frequently AOA: orbital axis orientation relative to CO called the posterior cranial base. (Ross and Ravosa, 1993). Prechordal cranial base: portion of the cra- BL1: Ba-PP ϩ PP-Sp (Ross and Ravosa, nial base anterior to sella; frequently called 1993; Ross and Henneberg, 1995). the anterior cranial base. BL2: Ba-S ϩ S-FC (Spoor, 1997). Telencephalon: forebrain, consisting of CBA1: Ba-S relative to S-FC (Lieberman paired olfactory lobes, the basal ganglia, and McCarthy, 1999). and the neocortex. CBA2: Ba-S relative to Sp-PS (Lieberman and McCarthy, 1999). LANDMARK DEFINITIONS CBA3: Ba-CP relative to S-FC (Lieberman and McCarthy, 1999). Ba, basion: midsagittal point on anterior CBA4: Ba-CP relative to Sp-PS (Lieberman margin of foramen magnum. and McCarthy, 1999). CP, clival point: midline point on basioccip- CO, clivus ossis occipitalis: endocranial line ital clivus inferior to point at which dorsum from Ba to spheno-occipital synchondrosis sellae curves posteriorly. (Ross and Ravosa, 1993). FC, foramen caecum: pit on cribriform plate External CBA (CBA5): angle between basion- between crista galli and endocranial wall of sphenobasion-hormion (Lieberman and Mc- frontal bone. Carthy, 1999). H, hormion: most posterior midline point on FM, foramen magnum: Ba-Op. vomer. Forel’s axis: from most antero-inferior point OA: supero-inferior midpoint between supe- on frontal lobe to most postero-inferior point rior orbital fissures and inferior rims of op- on occipital lobe (Hofer, 1969). tic canals; for mammals without completely Head-neck angle: orientation of head rela- enclosed orbits, OA is defined as inferior rim tive to neck in locomoting animals, calcu- of optic foramen. lated as neck inclination Ϫ orbit inclination OM: supero-inferior midpoint between (Strait and Ross, 1999). lower and upper orbital rims. IRE1: cube root of endocranial volume/BL 1 Op, opisthion: most posterior point in fora- (Ross and Ravosa, 1993). men magnum. IRE2: cube root of neocortical volume/BL 1 PMp, PM point: average of projected mid- (Ross and Ravosa, 1993). line points of most anterior point on lamina IRE3: cube root of telencephalon volume/BL of greater wings of sphenoid. 1 (Ross and Ravosa, 1993). IRE4: cube root of neocortical volume/palate PP, pituitary point: “the anterior edge of length (Ross and Ravosa, 1993). the groove for the optic chiasma, just in IRE5: cube root of endocranial volume/BL 2 front of the pituitary fossa” (Zuckerman, (McCarthy, 2001). 1955). Meynert’s axis: from ventral edge of junc- PS, planum sphenoideum point: most supe- tion between pons and medulla to caudal rior midline point on sloping surface in recess of interpeduncular fossa (Hofer, which cribriform plate is set. 1969). Ptm, pterygomaxillare: average of projected Neck inclination: orientation of surface of midline points of most inferior and posterior neck relative to substrate (Strait and Ross, points on maxillary tuberosities. 1999). S, sella: center of sella turcica, independent NHA: neutral horizontal axis of orbits; from of contours of clinoid processes. OM to OA (Enlow and Azuma, 1975). Sb, sphenobasion: midline point on spheno- Orbital axis orientation: line from optic fo- occipital synchondrosis on external aspect of ramen through superoinferior midpoint of clivus. orbital aperture (Ravosa, 1988). Sp, sphenoidale: most posterior, superior Orbit inclination: orientation relative to midline point of planum sphenoideum. substrate of a line joining superior and in- 120 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 ferior margins of orbits (Strait and Ross, 1993; O’Higgins, 2000). Ultimately, better 1999). information about the relationships be- PM plane, posterior maxillary plane: from tween cranial base morphology and the rest Ptm to PMp (Enlow and Azuma, 1975). of the skull may help to resolve a number of important phylogenetic and behavioral is- INTRODUCTION sues throughout primate evolution. The cranial base has important integra- The goals of this review are to provide a tive and functional roles in the skull, many background on key aspects of cranial base of which reflect its phylogenetic history as growth and development necessary to for- the oldest component of the vertebrate skull mulate or test hypotheses about the role of (de Beer, 1937). Architecturally, the cranial the cranial base in cranial growth, integra- base provides the platform upon which the tion, and function. Therefore, we review re- brain grows and around which the face cent research on cranial base variation, de- grows. In addition, the cranial base con- velopment, and evolution in primates, nects the cranium with the rest of the body: focusing on the major dimensions of the cra- it articulates with the vertebral column and nial base (especially width, length, and an- the mandible, provides conduits for all the gulation in the sagittal plane). Other, more vital neural and circulatory connections be- detailed aspects of cranial base anatomy tween the brain and the face and neck, and morphology, most notably the inner ear, houses and connects the sense organs in the were recently reviewed by Spoor and Zon- skull, and forms the roof of the nasophar- neveld (1998) and will not be covered in this ynx. The shape of the cranial base is there- review (see also Braga et al., 1999). Where fore a multifactorial product of numerous relevant, we have made an effort to include phylogenetic, developmental, and func- data from the few experimental studies on tional interactions. cranial base growth and function. Most ex- The importance of the cranial base is perimental research on the mammalian matched by several challenges that make it skull has focused on the face and neurocra- difficult to study. Because the cranial base nium; however, some of these studies pro- is difficult to access surgically, there have vide indirect clues on interrelationships been few experimental studies of cranial among the brain, cranial base, and face base growth and function. Also, a large pro- (e.g., Sarnat, 1988, 1999). Finally, we con- portion of the cranial base is not only com- clude with a short discussion of two main plex anatomically, but is also difficult to issues which we believe require further re- measure and/or see externally. In addition, search to address: what factors determine the cranial base in many fossils is missing, most of the variation in cranial base shape damaged, or unobservable without special among primates, and to what extent does technology. However, new developmental variation in cranial base form influence on- studies, and new techniques for imaging, togenetic and interspecific patterns of vari- have led to a modest renaissance of research ation in craniofacial morphology? on cranial base morphology (reviewed in ANATOMY AND DEVELOPMENT Spoor et al., 2000). In addition, new analyt- ical techniques which quantitatively com- A detailed understanding of the series of pare three-dimensional differences in form events and underlying mechanisms that 1 have opened up new possibilities for study- generate patterns of morphological varia- ing growth and variation in complex regions tion in the basicranium is vital for develop- such as the cranial base (Cheverud and ing and testing hypotheses about the cra- Richtsmeier, 1986; Bookstein, 1991; Lele, nial base’s role in craniofacial integration

1The term “pattern” here refers to a static description of a Please address all correspondence to: Daniel E. Lieberman, configuration or relationship among things, whereas “process” Department of Anthropology, George Washington University, refers to a series of events that occur during something’s forma- 2110 G St, Washington DC 20052. tion. Note that we do not define process here as a causal mech- E-mail: danliebgwu.edu; phone: 202-994-0873; fax: 202-994- anism. Most of the processes described here have multiple and 6097. hierarchical levels of causation which merit further study. D.E. Lieberman et al.] PRIMATE CRANIAL BASE 121

Fig. 1. Chondrocranium in Homo sapiens (after orbitosphenoid forms the lesser wing of the sphenoid; Sperber, 1989). A: Superior view of chondrocranial pre- the alisphenoid forms the greater wing of the sphenoid; cursors and ossification centers (after Sperber, 1989). the postsphenoid forms the sella turcica; the otic cap- Primordial cartilages are at right, and their cranial sule forms the petrous temporal; the parachordal forms base derivatives are on left. Note that the nasal capsule the basioccipital; and the occipital sclerotomes form the forms the ethmoid, the inferior concha, and the nasal exoccipital. B: Lateral view of chondrocranial precur- septum; the presphenoid forms the sphenoid body; the sors in a fetus 8 weeks i.u. and function. So we begin with a brief sum- From caudal to rostral these are: 1) four mary of cranial base embryology, fetal occipital condensations on either side of the growth, and postnatal growth. Most of the future brain stem derived from sclerotomic information summarized below derives from portions of postotic somites; 2) a pair of studies of human basicranial growth and parachordal cartilages on either side of the development; the majority of these patterns primitive notochord; 3) the otic capsules, ly- and processes are generally applicable to all ing lateral to the parachordal cartilages; 4) primates, but we tried to distinguish those the hypophyseal (polar) cartilages which that are unique to humans or other species. surround the anterior pituitary gland; 5–6) Further information is available in Bjo¨rk the orbitosphenoids (ala orbitalis/lesser (1955), Ford (1958), Scott (1958), Moore and wing of sphenoid) and alisphenoids (ala Lavelle (1974), Starck (1975), Bosma (1976), temporalis/greater wings of sphenoid) Moss et al. (1982), Slavkin (1989), Sperber which lie lateral to the hypophyseal carti- (1989), Enlow (1990), and Jeffery (1999), as lages; 7–8) the trabecular cartilages which well as the many references cited below. form the mesethmoid and, more laterally, the nasal capsule cartilages; and 9) the ala Development of the chondrocranium hypochiasmatica which, together with parts The human cranial base first appears in of the trabecular and orbitosphenoid carti- the second month of embryonic life as a lages, forms the presphenoid. narrow, irregularly shaped cartilaginous The chondrocranial precursors anterior to platform, the chondrocranium, ventral to the notochord (groups 5–9) derive solely the embryonic brain. The chondrocranium from segmented neural crest tissue (somito- develops between the base of the embryonic meres), while the posterior precursors brain and foregut about 28 days intra utero (groups 1–4) derive from segmented meso- (i.u.) as condensations of neural crest cells dermal tissue (somites) (Noden, 1991; Couly (highly mobile, pluripotent neurectodermal et al., 1993; Le Douarin et al., 1993). Con- cells that make up most of the head) and sequently, the middle of the sphenoid body paraxial mesoderm in the ectomeninx (a (the mid-sphenoidal synchondrosis) marks mesenchyme-derived membrane surround- the division between the anterior (prechord- ing the brain) (Sperber, 1989). By the sev- al) and posterior (postchordal) portions of enth week i.u., the ectomeninx has grown the cranial base that are embryologically around the base of the brain and differenti- distinct. Antero-posterior specification of ated into nine groups of paired cartilag- the segmental precursors of the cranial base enous precursors (Fig. 1A,B) (Kjaer, 1990). is complex and still incompletely known, but 122 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 appears to mostly involve the expression of tramembranous, including the squamous, the Hox and Dlx gene clusters (Lufkin et al., tympanic, and zygomatic regions (Shapiro 1992; Robinson and Mahon, 1994; Vielle- and Robinson, 1980; Sperber, 1989). The pe- Grosjean et al., 1997). For recent summa- trous and mastoid parts of the temporal ries of pattern formation and gene expres- form the inner ear from the otic capsule, and sion in the vertebrate cranial base, see the styloid process of the temporal ossifies Langille and Hall (1993) and Schilling and from cartilage in the second branchial arch. Thorogood (2000). The ethmoid, which is entirely endochon- At least 41 ossification centers, which be- dral in origin, forms the center of the ante- gin to appear in the chondrocranium about rior cranial floor, and most of the nasal cav- 8 weeks i.u., are responsible for the trans- ity from three ossification centers in the formation of the chondrocranium into the mesethmoid and nasal capsule cartilages basicranium (Sperber, 1989; Kjaer, 1990). (Hoyte, 1991). An additional cartilaginous These centers (Fig. 1B) form within a perfo- ossification center detaches from the ecteth- rated and highly irregularly shaped plat- moid to form a separate scrolled bone, the form known as the basal plate. In general, inferior nasal concha, inside the nasal cav- ossification begins with the mesodermally ity. derived cartilages toward the caudal end of Patterns and processes of basicranial the chondrocranium, and proceeds rostrally growth and laterally, eventually forming the four major bones that comprise the primate ba- In order to understand how the basicra- sicranium: the ethmoid, most of the sphe- nium grows and functions during the fetal noid, and parts of the occipital and temporal and postnatal periods, it is useful to keep in bones (which also include some intramem- mind three important principles of basicra- branous elements). The sequence in which nial development. First, the center of the the four bones of the cranial base ossify from basicranium (an oval-shaped region around the chondrocranium is complex, and still the sphenoid body) attains adult size and not entirely resolved (reviewed in Sperber, shape more rapidly than the anterior, pos- 1989; Williams et al., 1995; Jeffery, 1999), terior, and lateral portions, presumably be- but we highlight here the major steps, pro- cause almost all the vital cranial nerves and ceeding from caudal to rostral. The occipital major vessels perforate the cranial base in comprises four bones surrounding the fora- this region (Figs. 1A, 2) (Sperber, 1989). men magnum. The squamous portion is pri- Second, the prechordal (anterior) and post- marily intramembranous bone of the cra- chordal (posterior) cranial base grow some- nial vault, except for the nuchal region, what independently, perhaps reflecting which ossifies endochondrally from two sep- their distinct embryonic origins and their arate centers (Srivastava, 1992) and fuses different spatial and functional roles (out- with the lateral exoccipitals on either side of lined above). Third, most basicranial growth the foramen magnum that fuse with the in the three cranial fossae occurs indepen- basioccipital. The sphenoid body forms from dently (Fig. 2). The posterior cranial fossa, fusion of the presphenoids and basisphenoid which houses the occipital lobes and the around the pituitary, forming the sella tur- brain stem (the cerebellum and the medulla cica (“Turkish saddle”). The greater and oblongata), is bounded laterally by the pe- lesser wings of the sphenoid develop from trous and mastoid portions of the temporal the fusion of the alisphenoid and orbito- bone, and anteriorly by the dorsum sellae of sphenoid cartilages to the body (Kodama, the sphenoid. The butterfly-shaped middle 1976a–c; Sasaki and Kodama, 1976). Later, cranial fossa, which supports the temporal the medial and lateral pterygoid plates and lobes and the pituitary gland, is bounded portions of the greater wings ossify in- posteriorly by the dorsum sellae and the tramembraneously. The temporals, which petrous portions of the temporal, and ante- form much of the lateral aspect of the basi- riorly by the posterior borders of the lesser cranium, develop from approximately 21 os- wings of the sphenoid, and by the anterior sification centers, several of which are in- clinoid processes of the sphenoid. The ante- D.E. Lieberman et al.] PRIMATE CRANIAL BASE 123 in coronally oriented sutures such as the fronto-sphenoid; and 3) displacement in the midline of the cranial base from growth within the three synchondroses: the mid- sphenoid synchondrosis (MSS), the spheno- ethmoid synchondrosis (SES), and the sphe- no-occipital synchondrosis (SOS). During the fetal period in both humans and nonhu- man primates, the midline anterior cranial base grows in a pattern of positive allometry (mostly through ethmoidal growth) relative to the midline posterior cranial base (Ford, 1956; Sirianni and Newell-Morris, 1980; Sirianni, 1985; Anagnostopolou et al., 1988; Sperber, 1989; Hoyte, 1991; Jeffrey, 1999). During fetal growth, several key differences emerge between humans and other pri- mates in the relative proportioning of the posterior cranial fossa (Fig. 3). In humans, antero-posterior growth in the basioccipital is proportionately less than in the exoccipi- tal and squamous occipital posterior to the foramen magnum, whereas the pattern is apparently reversed in nonhuman pri- Fig. 2. Superior view of human cranial base (after mates, with proportionately more growth in Enlow, 1990). Left: Division between anterior cranial fossa (ACF), middle cranial fossa (MCF), and posterior the basioccipital (Ford, 1956; Moore and cranial fossa (PCF). Right: Locations of major foramina Lavelle, 1974). The nuchal plane rotates (in black), and distribution of resorptive growth fields downward to become more horizontal in hu- Ϫ ϩ (dark, with ) and depository growth fields (light, with ). mans, but rotates in the reverse direction to become more vertical in nonhuman pri- rior cranial fossa, which houses the frontal mates, apparently because of a growth field lobe and the olfactory bulbs, is bounded pos- reversal (Fig. 3). According to Duterloo and teriorly by the lesser wings of the sphenoid. Enlow (1970), the inside and outside of the Following its initial formation, the cranial nuchal plane in humans are resorptive and base grows in a complex series of events, depository growth fields, respectively; but in largely through displacement and drift (see nonhuman primates, the inside and outside Glossary). Four main types of growth occur of the nuchal plane are reported to be de- within and between the endocranial fossae: pository and resorptive growth fields, re- antero-posterior growth through displace- spectively. As a result, the foramen mag- ment and drift; medio-lateral growth num lies close to the center of the through displacement and drift; supero-in- basicranium in the human neonate and ferior growth through drift; and angulation more posteriorly in nonhuman primates (primarily flexion and extension). In order (Zuckerman, 1954, 1955; Schultz, 1955; to review how these types of growth occur, Ford, 1956; Biegert, 1963; Crelin, 1969). we will focus primarily on the sequence of Postnatally, the posterior cranial base events and patterns of basicranial growth in primarily elongates in the midline through humans and their major differences from deposition in the SOS and through posterior nonhuman primates. drift of the foramen magnum; more later- ally, the posterior cranial fossa elongates Antero-posterior growth. Basicranial through deposition in the occipitomastoid elongation during ontogeny occurs in three suture and through posterior drift. In all ways: 1) drift at the anterior and posterior primates, the basioccipital lengthens ap- margins of the cranial base; 2) displacement proximately twofold after birth, with rapid 124 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

Fig. 3. Midsagittal view of nonhuman primate (A) human (B), showing different patterns of drift of occipital, and position of foramen magnum, relative to overall cranial length in the Frankfurt horizontal. FM, center of the foramen magnum; OP (opisthocranium) and PR (prosthion) are, respectively the most posterior and anterior points on the skull in the Frankfurt horizontal. ϩ, depository surfaces; Ϫ resorptive surfaces. growth during the neural growth period elongates in concert with the frontal lobes of (e.g., up to approximately 6 years in hu- the brain, reaching approximately 95% of mans) and some additional elongation oc- its adult length by the end of the neural curring through the adolescent growth growth period (e.g., 6 years in humans, 3 spurt (Ashton and Spence, 1958; Scott, years in chimpanzees, and 1.2 years in ma- 1958; Riolo et al., 1974; Sirianni and Swin- caques) (Scott, 1958; Sirianni and Newell- dler, 1979; Sirianni, 1985). The SOS con- Morris, 1978; Sirianni and Van Ness, 1978; tributes to roughly 70% of posterior cranial Lieberman, 1998). Postnatal anterior cra- base elongation in macaques (Sirianni and nial base elongation can occur in the SES (in Van Ness, 1978). The rest of posterior basi- the midline), through displacement in the cranial growth in nonhuman primates oc- sphenoid-frontal suture, and through drift curs through posterior drift of the foramen of the anterior margin of the frontal bone. In magnum, which has been shown by fluoro- humans, however, the SES remains active chrome dye labeling experiments to migrate and unfused until 6–8 years after birth, caudally in nonhuman primates through re- when the brain has completed most of its sorption at its posterior end and deposition growth, but the SES apparently fuses near at its anterior end (Michejda, 1971; Giles et birth in nonhuman primates (Michejda and al., 1981). In contrast, the foramen magnum Lamey, 1971). These differences in the tim- remains in the center of the human skull ing and sequence of synchondroseal activity base, roughly halfway between the most an- and fusion may be related to the different terior and posterior points of the skull relative contributions of the lesser wings of (Lugoba and Wood, 1990). The posterior cra- the sphenoid and the frontal to the anterior nial base in H. sapiens still elongates during cranial floor in humans and nonhuman pri- postnatal growth, but to a lesser degree mates. Although there is some intraspecific than in nonhuman primates. variation, the lesser wing of the sphenoid in Postnatal elongation in the anterior cra- humans tends to comprise approximately nial base is somewhat more complex be- one third of the cranial floor, extending all cause of its multiple roles in neural and the way to the cribriform plate; in nonhu- facial growth. The anterior cranial base man primates, the cribriform usually lies (measured from sella to foramen caecum) entirely within the ethmoid (Fig. 4), and the D.E. Lieberman et al.] PRIMATE CRANIAL BASE 125

Fig. 4. Superior view of cranial base in Homo sapiens (left) and Pan troglodytes (right) (after Aiello and Dean, 1991). FC, foramen, caecum; PS, planum sphenoideum point; SP, sphenoidale; S, sella. Note similar orientation of the inferior petrosal posterior surface (PPip) in the two species (data from Spoor, 1997). In addition, the lesser wing of the sphenoid and the cribriform plate comprise a much greater percentage of the midline anterior cranial base in humans than in chimpanzees. lesser wing of the sphenoid makes up less ious interactions with neurocranial and fa- than one tenth of the cranial floor (Van der cial shape (Lieberman et al., 2000; see be- Linden and Enlow, 1971; Aiello and Dean, low). The increases in width of the anterior 1990; McCarthy, 2001). Differences in the and posterior cranial fossae occur primarily sequence of synchondroseal fusion may also from drift (in which the external and inter- be related to differences in the timing and nal surfaces of the squamae are depository nature of cranial base angulation in human and resorptive, respectively), and from in- vs. nonhuman primates (Jeffery, 1999; see tramembranous bone growth in sutures below). with some component of lateral orientation, While the anterior cranial base grows such as the fronto-ethmoid and occipito- solely during the neural growth phase (it mastoid sutures (Sperber, 1989). Lateral reaches adult size at the same time as the growth in the middle cranial fossa is slightly brain), the more inferior portions of the more complicated. The sphenoid body does anterior cranial base continue to grow as not widen much (Kodama, 1976a,b; Sasaki part of the face after the neural growth and Kodama, 1976). Instead, most increases phase, forming the ethmomaxillary com- in middle cranial fossa width presumably plex (Enlow, 1990). This complex grows occur in the spheno-temporal suture and downward and forward mostly through through lateral drift of the squamous por- drift and displacement. In addition, the tions of the sphenoid. sphenoid sinus drifts anteriorly. Since the Increases in cerebellum and brain-stem ethmoid (with the exception of the cribri- size have been implicated in changes in the form plate) primarily grows as part of the ethmomaxillary complex, its postnatal orientation of the petrous pyramids (Fig. 4), growth is most properly treated in a re- which are more coronally oriented exter- view of facial growth. nally (but not internally) in humans than in nonhuman primates (Dean, 1988). Spoor Medio-lateral growth. How the cranial (1997) found that petrous pyramid orienta- base widens is important because of its var- tion in a broad interspecific sample of pri- 126 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 mates was significantly negatively corre- Angulation. Angulation of the cranial lated with relative brain size (r ϭϪ0.85, base occurs when the prechordal and post- P Ͻ 0.001) but not with the cranial base chordal portions of the basicranium flex or angle. However, Jeffery (1999) found that extend relative to each other in the midsag- petrous pyramid orientation is independent ittal plane (technically, flexion and exten- of relative brain size in fetal humans (dur- sion describe a series of events in which the ing the second trimester). angle between the inferior or ventral sur- faces of the cranial base decrease or in- Supero-inferior growth. Most brain crease, respectively). Angulation has been growth apparently causes the neurocra- the subject of much research because flexion nium and parts of the basicranium to grow and extension of the cranial base affect the superiorly, anteriorly, and laterally (de relative positions of the three endocranial Beer, 1937). However, the endocranial fos- fossae, thereby influencing a wide range of sae also become slightly deeper through spatial relationships among the cranial drift because most of the endocranial floor is base, brain, face, and pharynx (see below). resorptive, while the inferior side of the ba- Although all measures of cranial base an- sicranium is depository (Fig. 2) (Duterloo gle are similar in that they attempt to quan- and Enlow, 1970; Enlow, 1990). The en- tify the overall degree of angulation in the docranial margins between the fossae that midsagittal plane between the prechordal separate the different portions of the brain and postchordal portions of the cranial base, (the petrous portion of the temporal and the there have been at least 17 different mea- lesser wing of the sphenoid) do not drift surements used since Huxley (1867) first inferiorly because they remain depository attempted to quantify the angle (reviewed surfaces (Enlow, 1976). Differences in drift in Lieberman and McCarthy, 1999, and most likely reflect variation in the relative summarized in Table 1). Many of these an- size of the components of the brain in con- gles differ considerably in how they mea- junction with other spatial relationships sure the prechordal and postchordal planes among components of the skull. In particu- and, consequently, the point of intersection lar, inferior drift of the anterior cranial between them. Figure 5 illustrates some of these angles. The postchordal plane is most fossa is presumably minimal because it commonly defined using two landmarks, would impinge upon the orbits and nasal usually basion and sella, or using the line cavity that lie immediately below. The only created by the dorsal surface of the basioc- exception is the cribriform plate which cipital clivus (the clival line). The pre- drifts inferiorly, slightly in humans (Moss, chordal plane has been measured in more 1963), but sometimes forming a “deep olfac- diverse ways. Historically, the most com- tory pit” in many species of nonhuman pri- mon plane is defined by two landmarks, mates (Cameron, 1930; Aiello and Dean, sella and nasion. The sella-nasion line is 1990). Inferior drift of the middle cranial problematic, however, because nasion is ac- fossa presumably reflects inferiorly directed tually part of the face and moves anteriorly growth of the temporal lobes, but this hy- and inferiorly relative to the cranial base pothesis has not been tested. Likewise, in- throughout the period of facial growth ferior drift in the posterior cranial fossa, (Scott, 1958; Enlow, 1990). Recently, most which is shallow in most nonhuman pri- researchers have defined the prechordal mates, is hypothesized to be a function of plane either from sella to the foramen cae- the size of the occipital lobes, the cerebel- cum (a pit on the anterior end of the cribri- lum, and the brain stem below the tento- form plate between the crista galli between rium cerebelli. Note that cranial base flex- frontal squama), or using the planum sphe- ion during growth, which occurs uniquely in noideum which extends from sphenoidale humans (see below), complements inferior (the most postero-superior point on the tu- drift in the posterior cranial fossa by moving berculum sellae) to the planum sphenoi- the floor of the posterior cranial fossa more deum point (defined as the most anterior below the middle cranial fossa. point on the surface of the midline anterior D.E. Lieberman et al.] PRIMATE CRANIAL BASE 127

TABLE 1. Commonly used measures of midsagittal cranial base angle Posterior (P) and anterior (A) Angle planes used References External cranial base angle P: basion-sella Bjo¨rk, 1951, 1955; Stamrud, 1959 Nasion-sella-basion A: sella-nasion Melsen, 1969; George, 1978 Landzert’s sphenoidal angle P: clival plane Landzert, 1866; Biegert, 1957; Clivus/clival angle A: ethmoidal plane (planum Moss, 1958; Hofer, 1957; CBA4, planum angle sphenoideum/ale) Angst, 1967; Cartmill, 1970; Dmoch, 1975; Ross and Ravosa, 1993; Ross and Henneberg, 1995 Clivus angle P: clival plane George, 1978 A: sphenoidale-fronton Ethmoidal angle P: basion-sella Stamrud, 1959 Internal cranial base angle A: sella-ethmoidale Spheno-ethmoidal angle P: basion-prosphenion Huxley, 1867; Topinard, 1890; Duckworth, 1904; Cameron, 1924; Zuckerman, 1955 Cameron’s cranio-facial axis P: basion-pituitary point Cameron, 1924, 1925, 1927a,b, A: pituitary point-nasion 1930 Basioccipito-septal angle P: basion-pituitary point Ford, 1956 A: pituitary point-septal point Bolton’s external cranial base angle P: Bolton point-sella Brodie, 1941, 1953 A: sella-nasion Anterior cranial base angle P: clival plane Scott, 1958; Cramer, 1977 A: prosphenion-anterior cribriform point (ACP) Internal cranial base angle, basion- P: basion-sphenoidale George, 1978 sphenoidale-fronton A: sphenoidale-fronton Internal cranial base angle, basion- P: basion-sella George, 1978 sella-fronton A: sella-fronton Internal cranial base angle, basion- P: basion-sella Cousin et al., 1981; Spoor, 1997 sella-foramen caecum CBA1 A: sella-foramen caecum Lieberman and McCarthy, 1999 External cranial base angle, nasion- P: basion-sphenoidale George, 1978 sphenoidale-basion A: sphenoidale-nasion Orbital angle P: clival plane Moss, 1958 A: plane of superior orbital roof Planum angle (PANG) P: basion-sella Anto´n, 1989 A: planum sphenoidale Orbital angle (OANG) P: basion-sella Anto´n, 1989 A: plane of superior orbital roof cranial base posterior to the cribriform primates with other mammals (McCarthy, plate). in press). In humans and some anthropoids, Since different lines emphasize different the cribriform plate lies in approximately aspects of cranial base anatomy, the choice the same plane as the planum sphenoi- of which cranial base angle to use is largely deum, but in other anthropoids the cribri- dependent on the question under study. form plate lies in a deep olfactory pit within Both postchordal lines tend to yield roughly the ethmoidal notch of the frontal bone (Fig. similar results (George, 1978; Lieberman 6) (Aiello and Dean, 1990; Ravosa and Shea, and McCarthy, 1999), but the prechordal 1994). Moreover, in strepsirrhines and lines can be substantially different. In par- other mammals with more divergent orbits ticular, S-FC spans the entire length of the and projecting snouts, the cribriform plate anterior cranial base, including the cribri- typically lies at a steep angle relative to the form plate, whereas the planum sphenoi- planum sphenoideum (Cartmill, 1970). deum does not measure the portion of the Variations in cranial base angulation cranial base that includes the cribriform need to be considered in both comparative plate. Because of variation in the growth and ontogenetic studies. For example, it is and position of the cribriform plate, these well known that humans have a much more differences affect comparisons of anthro- flexed cranial base than other primates, but poids with strepsirrhines, or comparisons of it is not well appreciated that the human 128 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

Fig. 5. Major cranial base angles used in this review, illustrated in a human cranium. CBA1 is the angle between the basion-sella (Ba-S) line and the sella-foramen (S-FC) caecum line. CBA4 is the angle between the midline of the postclival plane, and the midline of the planum sphenoideum.

Fig. 6. Lateral radiographs of hemisected baboon cranium (A) and human cranium (B). Note different orientation and position of the cribriform plate (CP) relative to the planum sphenoideum (PS) in the two species. cranial base flexes postnatally, while the mologous differences exist because changes nonhuman primate cranial base extends in the cranial base angle can occur through postnatally, possibly at different locations different growth processes (e.g., drift, dis- (Hofer, 1960; Sirianni and Swindler, 1979; placement) at different locations. The actual Cousin et al., 1981; Lieberman and Mc- cellular processes that result in angulation, Carthy, 1999). These potentially nonho- however, are not completely understood. D.E. Lieberman et al.] PRIMATE CRANIAL BASE 129 Some researchers (Scott, 1958; Giles et al., A few experimental studies provide evi- 1981; Enlow, 1990) suggest that changes in dence for the presence of complex interac- cranial base angulation occur interstitially tions between the brain and cranial base within synchondroses through a hinge-like synchondroses that influence variation in action. If so, flexion would result from in- the cranial base angle. DuBrul and Laskin creased chrondrogenic activity in the supe- (1961), Moss (1976), Bu¨ tow (1990), and Rei- rior vs. inferior aspect of the synchondrosis, denberg and Laitman (1991) all inhibited while extension would result from increased growth in the SOS in various animals chrondrogenic activity in the inferior vs. su- (mostly rats), causing a more flexed cranial perior aspect of the synchondrosis. Experi- base, presumably through inhibition of cra- mental growth studies in macaques, which nial base extension. In most of these stud- labeled growth using flurochrome dyes, ies, experimentally induced kyphosis of the show that angulation also occurs through basicranium was also associated with a drift in which depository and resorptive shorter posterior portion of the cranial base, growth fields differ on either side of a syn- and a more rounded neurocranium (see be- chondrosis, causing rotations around an low). Artificial deformation of the cranial axis through the synchondrosis (Michejda, vault also causes slight but significant in- 1971, 1972a; Michejda and Lamey, 1971; creases in cranial base angulation (Anto´n, Giles et al., 1981). All three synchondroses 1989; Kohn et al., 1993). However, no con- are involved in prenatal angulation (Hofer, trolled experimental studies have yet exam- 1960; Hofer and Spatz, 1963; Sirianni and ined disruptions to the other cranial base Newell-Morris, 1980; Diewert, 1985; Ana- synchondroses. In addition, there have been few controlled studies of the effect of in- gastopolou et al., 1988; Sperber, 1989; van creasing brain size on cranial base angula- den Eynde et al., 1992); however, the extent tion. In one classic experiment, Young to which each synchondrosis participates in (1959) added sclerosing fluid into the cra- postnatal flexion and extension is poorly nial cavity in growing rats, which caused known, and probably differs between hu- enlargement of the neurocranium with little mans and nonhuman primates. The SOS, effect on angular relationships in the cra- which remains active until after the erup- nial base. Additional evidence for some de- tion of the second permanent molars, is gree of independence between the brain and probably the most active synchondrosis in cranial base during development is provided generating angulation in primates (Bjo¨rk, by microcephaly and hydrocephaly, in 1955; Scott, 1958; Melsen, 1969). The MSS which cranial base angles tend to be close to fuses prior to birth in humans (Ford, 1958), those of humans with normal encephaliza- but may also be important in nonhuman tion (Moore and Lavelle, 1974; Sperber, primates (Scott, 1958; Hofer and Spatz, 1989). 1963; Michejda, 1971, 1972a; but see Lager, Important differences in cranial base an- 1958; Melsen, 1971; Giles et al., 1981). Fi- gulation among primates exist in terms of nally, the SES fuses near birth in nonhu- the ontogenetic pattern of flexion and/or ex- man primates, and remains active only as a tension, which presumably result from dif- site of cranial base elongation in humans ferences in the rate, timing, duration, and during the neural growth period (Scott, sequence of the growth processes outlined 1958; Michejda and Lamey, 1971). Other above. Jeffery (1999) suggested that, prena- ontogenetic changes in the cranial base an- tally, the basicranium in humans initially gle (not necessarily involved in angulation flexes rapidly during the period of rapid itself) include posterior drift of the foramen hindbrain growth in the first trimester, re- magnum (see above), inferior drift of the mains fairly stable during the second tri- cribriform plate relative to the anterior cra- mester, and then extends during the third nial base (Moss, 1963), and remodeling of trimester in conjunction with facial exten- the sella turcica, which causes posterior sion, even while the brain is rapidly increas- movement of the sella (Baume, 1957; Sha- ing in size relative to the rest of the cranium piro, 1960; Latham, 1972). (see also Bjo¨rk, 1955; Ford, 1956; Sperber, 130 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

Fig. 7. Changes in the angle of the cranial base (CBA1 and CBA4) in Homo sapiens (left) and Pan troglodytes (right) (after Fig. 6 in Lieberman and McCarthy, 1999). For both species, means (circles) and standard deviations (whiskers) are summarized by the mean chronological age of each dental stage. Note that the human cranial base flexes rapidly during stage I and then remains stable, whereas the chimpanzee cranial base extends gradually through stage V. *P Ͻ 0.05.

1989; van den Eynde et al., 1992). Little is The polyphasic and multifactorial nature known about prenatal cranial base angula- of cranial base angulation during ontogeny tion in nonhuman primates; however, major and the ontogenetic contrasts between the differences between humans and nonhu- relative contribution of underlying factors mans appear during the fetal and postnatal in humans and nonhumans provide some periods of growth. As Figure 7 illustrates, clues for understanding the complex, multi- the human cranial base flexes rapidly after ple interactions between cranial base angu- birth, almost entirely prior to 2 years of age, lation, encephalization, and facial growth. and well before the brain has ceased to ex- There is abundant evidence based on inter- pand appreciably (Lieberman and Mc- specific studies (see below) that variation in Carthy, 1999). In contrast, the nonhuman cranial base angle in primates is associated primate cranial base extends gradually af- in part with variation in brain volume rela- ter birth throughout the neural and facial tive to the length of the cranial base. How- growth periods, culminating in an acceler- ever, relative encephalization accounts for ated phase during the adolescent growth only 36% of the variation in cranial base spurt (Hofer, 1960; Heintz, 1966; Sirianni angle among anthropoids, and both inter- and Swindler, 1979; Cousin et al., 1981; specific and ontogenetic data suggest that a Lieberman and McCarthy, 1999). large proportion of the variation in cranial D.E. Lieberman et al.] PRIMATE CRANIAL BASE 131 base angle among primates must also be lationships between the cranial base and related to variation in facial growth, orbit the face are discussed below. orientation, and relative orbit size (Ross and Brain size and cranial base angle Ravosa, 1993; Ravosa et al., 2000a). As noted above, the ontogenetic pattern of pre- Numerous anatomists have posited a re- natal cranial base angulation in humans is lationship between brain size and basicra- largely unrelated to the rate at which the nial angle (e.g., Virchow, 1857; Ranke, 1892; brain expands (Jeffery, 1999). In addition, Cameron, 1924; Bolk, 1926; Dabelow, 1929, the nonhuman primate cranial base angle 1931; Biegert, 1957, 1963; Delattre and Fe- (regardless of whether the cribriform plate nart, 1963; Hofer, 1969; Gould, 1977; Ross is included in the measurement) mostly ex- and Ravosa, 1993; Ross and Henneberg, tends during the period of facial growth, 1995; Spoor, 1997; Strait, 1999; Strait and after the brain has ceased to expand Ross, 1999; McCarthy, 2001). The most (Lieberman and McCarthy, 1999). There- widely accepted of these hypotheses is that fore, we will next explore in greater depth the angle of the midline cranial base in the the relationship between cranial base angle, sagittal plane correlates with the volume of brain size, relative orbit size and position, the brain relative to basicranial length facial orientation, and other factors such as (DuBrul and Laskin, 1961; Vogel, 1964; pharyngeal shape and facial projection. Riesenfeld, 1969; Gould, 1977). This hypoth- esis is supported by independent analyses of ASSOCIATIONS BETWEEN CRANIAL different measures of basicranial flexion BASE AND BRAIN across several interspecific samples of pri- mates (Ross and Ravosa, 1993; Spoor, 1997; Because of the close relationship between McCarthy, 2001) (Fig. 8): the adult midline the brain and the cranial base during devel- cranial base is significantly and predictably opment (see above), the hypothesis that more flexed in species with larger endocra- brain size and shape influence basicranial nial volumes relative to basicranial length. morphology is an old and persistent one. In particular, the analysis by Ross and Ra- The bones of the cranial cavity, including vosa (1993) of a broad interspecific sample the cranial base, are generally known to of primates found that the correlation coef- conform to the shape of the brain, but the ficient between relative encephalization specifics of this relationship and any recip- (IRE1, see below) and cranial base angle rocal effects of cranial base size and shape (CBA4, see below) was 0.645 (P Ͻ 0.001), on brain morphology remain unclear. For explaining approximately 40% of the varia- example, the human basicranium is flexed tion in cranial base angle. when it first appears in weeks 5 and 6 be- Attempts to extend this relationship to cause in the fourth week, the neural tube hominins have proved controversial. Ross bends ventrally at the cephalic flexure and Henneberg (1995) reported that Homo (O’Rahilly and Mu¨ ller, 1994). The para- sapiens have less flexed basicrania than chordal condensations caudal to the ce- predicted by either haplorhine or primate phalic flexure are therefore in a different regressions. They posited that spatial con- anatomical plane than the more rostral pre- straints limit the degree of flexion possible, chordal condensations (which develop by and that humans accommodate further week 7). However, as noted above, it is dif- brain expansion relative to cranial base ficult to attribute many of the subsequent length through means other than flexion, changes in prenatal chondrocranial or basi- such as superior, posterior, and lateral neu- cranial angulation (or other measures of the rocranial expansion. In contrast, Spoor base) as responses solely to changes in brain (1997), using different measures of flexion morphology. and relative brain size taken on a different Here we review several key aspects of the sample, found H. sapiens to have the degree association between brain and cranial base of flexion expected for its relative brain size. morphology, as derived from interspecific Spoor (1997) used the angle basion-sella- analyses of adult specimens. Structural re- foramen caecum (CBA1) to quantify basi- 132 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

Fig. 8. Bivariate plot of CBA4 against IRE5. These variables are significantly correlated across Primates (r ϭϪ0.621; P Ͻ 0.05) and Haplorhini (r ϭϪ0.636; P Ͻ 0.05). cranial flexion, and the length of these line Henneberg (1995) (n ϭ 64 species). We segments (thereby including cribriform therefore reanalyzed the relationships be- plate length) to quantify basicranial length tween flexion and relative brain size in a (BL2), whereas Ross and Henneberg (1995) large interspecific primate sample, utilizing measured flexion using CBA4 and relative both CBA1 and CBA4 as measures of flexion brain size using IRE1 (endocranial vol- and IRE5 as a measure of relative brain 0.33 ume /BL1). size.2 IRE5 incorporates the more appropri- The two most likely sources of the discrep- ate basicranial length that includes cribri- ancy between the results of Spoor (1997) vs. form plate length (see Glossary and Mea- Ross and Henneberg (1995) were the differ- surement Definitions). The human value for ent measures and different samples. Mc- CBA1 falls within the 95% confidence limits Carthy (2001) has since investigated the in- of the value predicted for an anthropoid of fluence of different measures, noting that its relative brain size, but the human value the measure of basicranial length by Ross and Henneberg (1995) excluded the horizon- for CBA4 does not. These results corrobo- tally oriented cribriform plate that contrib- rate those of McCarthy (2001): the degree of utes to basicranial length in anthropoids basicranial flexion in humans is not signif- more than in strepsirrhines. McCarthy icantly less than expected using CBA1, but (2001) also demonstrated that the frontal is less than expected using CBA4. Thus hu- bone contributes less to midline cranial base mans may or may not have the degree of length in hominoids, especially humans, causing BL1 to underestimate midline basi- cranial length relative to endocranial vol- 2Measurements were taken on radiographs of nonhuman pri- ume compared to other anthropoids. How- mates from Ravosa (1991b) and Ross and Ravosa (1993), and on 98 Homo sapiens from Ross and Henneberg (1995). RMA slopes ever, the data sets of both McCarthy (2000) were calculated for nonhominin primates, and the 95% bootstrap and Spoor (1997) were small (n ϭ 17 spe- confidence limits for the value of y predicted for humans were calculated according to Joliceur and Mosiman (1968), using soft- cies) in comparison with that of Ross and ware written by Tim Cole. D.E. Lieberman et al.] PRIMATE CRANIAL BASE 133

TABLE 2. Variance components for indices of relative brain size and measures of flexion across primates1 IRE1 IRE5 CBA4 CBA1

Level N %Neff %Neff %Neff %Neff Infraorder 2 12 0.24 48 0.94 0 0 52 1.05 Superfamily 6 22 1.34 10 0.62 34 2.07 0 0.00 Family 15 54 8.16 16 2.44 44 6.56 35 5.19 Genus 60 13 7.81 22 12.99 17 10.26 8 4.74 Species 62 1 0.78 3 2.38 5 3.10 5 3.25

Total Neff 18.33 17.38 21.99 14.23 df 16.00 15.00 20.00 12.00 1 Maximum likelihood variance components were calculated using mainframe SAS (proc ϭ varcomp). %, percentage of variance at each taxonon 1 mic level; Neff, effective N at each level; Total Neff, total effective N for each variable. Bivariate comparisons utilize lowest Neff of the pair.

TABLE 3. Correlation coefficients for primates and haplorhini1

Variables CBA4 N (P)dfeff (P) CBA1 N (P)dfeff (P) Primates IRE1 Ϫ0.783 60 (Ͻ0.001) 14 (0.01) Ϫ0.672 60 (Ͻ0.001) 10 (0.05) IRE5 Ϫ0.621 60 (Ͻ0.001) 13 (0.05) Ϫ0.790 62 (Ͻ0.001) 10 (0.01) Haplorhini IRE1 Ϫ0.813 51 (Ͻ0.001) 9 (0.01) Ϫ0.641 51 (Ͻ0.001) 9 (0.05) IRE5 Ϫ0.636 51 (Ͻ0.001) 10 (0.05) Ϫ0.548 51 (Ͻ0.001) 14 (0.05) 1 Ϫ N, total N; deff,Neff 2, effective degrees of freedom for each comparison. Bivariate comparisons utilize lowest Neff of the pair.

flexion expected for their relative brain size, the method of Smith (1994) is conservative depending on which measures are used. and the correlations that survive these cor- One problem with the above studies is rected degrees of freedom are robust, al- that they do not consider the potential role though of relatively low magnitude. Across of phylogenetic effects on these correlations primates and haplorhines, both CBA4 and (Cheverud et al., 1985; Felsenstein, 1985). CBA1 are significantly correlated (P Ͻ 0.05) Accordingly, the above data were reana- with IRE5 (Fig. 8; Table 2). These results lyzed using the method of Smith (1994) for corroborate the results of Ross and Ravosa 3 adjusting degrees of freedom. Table 2 pre- (1993), but with a more appropriate mea- sents the percentage of total variance dis- sure of basicranial length incorporated into tributed at each taxonomic level within the the measure of relative brain size. This con- order Primates. Table 3 presents the corre- firms that brain size relative to basicranial lation coefficients for comparisons of CBA length is significantly correlated with basi- and IRE for Primates and Haplorhini, along cranial flexion, but that the correlations are with sample sizes, degrees of freedom ad- not particularly strong, indicating that justed for phylogeny (dfeff), and their asso- there may be other important influences on ciated P-values (for which strepsirrhines the degree of basicranial flexion (see below). had no significant correlations). Examina- Most hypotheses explaining basicranial tion of the variance components in Table 2 flexion have focused on increases in relative shows that the relationship between cranial brain size as the variable driving flexion. base angle and relative brain size is subject However, as Strait (1999) has noted, it is to significant phylogenetic effects. However, important to consider the scaling relation- ships of basicranial length and brain size. Using interspecific data from Ross and Ra- 3Unlike methods such as “independent contrasts” (e.g., Purvis and Rambaut, 1995), Smith’s method uses values for variables in vosa (1993) in conjunction with other stud- just terminal taxa, therefore avoiding potentially spurious esti- mates of these values for ancestral nodes. Smith’s method is also ies, Strait (1999) found that basicranial more robust when five or fewer taxonomic levels are considered length scales with negative allometry and is less affected by arbitrary taxonomic groupings (Nunn, 1995). We also used the maximum likelihood method for calcu- against body mass and telencephalon vol- lating variance components rather than a nested ANOVA ume (results confirmed here using BL2 in- method because maximum likelihood does not generate negative variance components. stead of BL1; see Table 4), and BL2 also 134 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

TABLE 4. Reduced major axis regression equations for scaling of basicranial dimensions against neural variables1 95% CI Comparison Intercept Slope of slope Scaling3 Nr BL2 vs. Body mass 0.908 0.654 0.035 Ϫve 61 0.978 Telencephalon 0.541 0.742 0.091 Ϫve 33 0.960 Brain stem 0.404 1.123 0.100 ϩve/Iso 33 0.975 Neurocranial volume 1.270 0.734 0.056 Ϫve 62 0.962 Palate (Pros-PNS) 1.394 0.642 0.032 Ϫve 58 0.929 Anterior face (Pros-Nas) 1.623 0.577 0.028 Ϫve 58 0.933 Upper toothroow 1.425 0.666 0.035 Ϫve 58 0.921 Geometric mean2 0.951 0.750 0.023 Ϫve 58 0.972 Ba-S vs. Body mass 0.380 0.759 0.056 Ϫve 63 0.958 Brain stem Ϫ0.226 1.354 0.161 ϩve 33 0.946 Telencephalon 0.313 0.908 0.135 Iso 33 0.924 Cerebellum 0.105 0.953 0.111 Iso 33 0.948 Infratentorial brain Ϫ0.064 1.044 0.123 Iso 33 0.947 Palate (Pros-PNS) 0.595 0.757 0.040 Ϫve 58 0.917 Anterior face (Pros-Nas) 0.862 0.681 0.037 Ϫve 58 0.914 Upper toothroow 0.626 0.787 0.043 Ϫve 58 0.924 Geometric mean2 0.067 0.886 0.034 Ϫve 58 0.957 S-FC vs. Ba-S 0.473 0.759 0.063 Ϫve 33 0.949 Body mass 0.748 0.587 0.040 Ϫve 56 0.965 Brain stem 0.249 1.070 0.101 Iso 33 0.971 Telencephalon 0.378 0.715 0.082 Ϫve 33 0.963 Cerebellum 0.516 0.749 0.079 Ϫve 33 0.964 Infratentorial brain 0.381 0.822 0.085 Ϫve 33 0.965 Palate (Pros-PNS) 1.382 0.581 0.032 Ϫve 58 0.912 Anterior face (Pros-Nas) 1.586 0.523 0.027 Ϫve 58 0.922 Upper toothroow 1.406 0.604 0.035 Ϫve 58 0.900 Geometric mean2 0.977 0.680 0.026 Ϫve 58 0.958 1 All volumetric and mass variables converted to cube roots. All calculations in log-log space (base 10). Calculations with facial dimensions do not include humans; all other calculations include humans. 2 Geometric mean of the following measures: palate length, palate breadth, anterior face length, maxillary postcanine toothrow length, outer biorbital breadth, bizygomatic breadth, basicranial length, and lower skull length. Measures of brain volume from Stephan et al. (1981), measures of body mass from Smith and Jungers (1994), and measures of facial size derive from the same skulls from which the radiographs were taken. 3 Ϫve, negative; ϩve, positive; Iso, isometric. scales with negative allometry against mea- relative shortening of the anterior cranial sures of facial size (Table 4). The only vari- base. able that scales close to isometry with basi- Brain shape and cranial base angle cranial length is brain-stem volume, which is isometric with BL1 and scales close to Given the close anatomical relationship isometry with BL2 (Table 4). Intuitively this between the brain and basicranium, it isometry makes sense, because the brain seems intuitive that the shapes of the two stem rests on the basicranium. However, should be related, but testing this hypothe- the posterior basicranium (Ba-S), which sis in a controlled fashion has been difficult. predominantly underlies the brain stem, The best evidence for the presence of inter- scales with positive allometry to brain-stem actions between brain shape and the cranial volume, whereas the anterior cranial base base came from studies of artificial cranial length scales isometrically with brain-stem vault deformation and from the effects of volume. Notably, the anterior cranial base closing various cranial vault sutures on the always shows lower slopes than the poste- cranial base. The effects of head-binding are rior cranial base, suggesting that the strong difficult to interpret without precise data on negative allometry of cranial base length the timing and forces used to deform the relative to neural variables, and possibly skull. Nevertheless, antero-posterior head- flexion, is disproportionately attributable to binding tends to cause lateral expansion of D.E. Lieberman et al.] PRIMATE CRANIAL BASE 135

Fig. 9. Bivariate plot of the measure by Hofer (1969) dulla to the caudal recess of the interpeduncular fossa. of basicranial flexion and CBA4 against his measure of The data of Hofer (1969) measure anterior angles be- brain flexion. Hofer’s brain angle is the anterior angle tween lines, rather than the inferior angles favored by between Forel’s axis, from the most antero-inferior recent workers (e.g., Ross and Ravosa, 1993). The plot- point on the frontal lobe to the most postero-inferior ted data therefore represent the complement of Hofer’s point on the occipital lobe, and Meynert’s axis, from the angles. ventral edge of the junction between the pons and me- the cranial base along with a slight increase the inferior surface of the cerebral hemi- in CBA; conversely, annular head-binding spheres; and Meynert’s axis, from the ven- tends to cause medio-lateral narrowing and tral edge of the junction between the pons antero-posterior elongation of the cranial and medulla to the caudal recess of the in- base, also with a slight increase in CBA terpeduncular fossa, quantifying the orien- (Anto´n, 1989; Cheverud et al., 1992; Kohn et tation of the brain stem. Hofer (1965) also al., 1993). Natural or experimentally in- measured the angle of the midline cranial duced premature closure of sutures (synos- base using a modified version of the angle of toses) in the cranial vault have similarly Landzert (1866), similar to the CBA4 used predictable effects. For example, bilateral by Ross and Ravosa (1993). coronal synostoses cause antero-posterior Figure 9, a plot of the measure by Hofer of shortening of the cranial base (Babler, 1989; basicranial angle against his measure of David et al., 1989), and unilateral coronal brain angle, illustrates that these variables synostoses (plagiocephaly) cause marked are highly correlated and scale isometrically asymmetry in the cranial vault, cranial with each other (i.e., have a slope of 1.0). As base, and face. the cerebrum flexes on the brain stem, the Interspecific analyses of the relationship planum sphenoideum flexes relative to the between brain shape and cranial base shape clivus. The explanation of Hofer (1969) for in primates are rare. Hofer (1965, 1969) this phenomenon is that the telencephalon measured the orientation of the cerebral becomes more spherical as it enlarges, to hemispheres relative to the brain stem in minimize surface area relative to volume. primates using two axes: Forel’s axis, from An alternative hypothesis is that increasing the most antero-inferior point on the frontal the antero-posterior diameter of the head lobe to the most postero-inferior point on the “would be disastrous, making larger ani- occipital lobe, measuring the orientation of mals unusually long-headed, and would pro- 136 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

TABLE 5. Correlation coefficients for flexion vs. measures of relative brain size

NNeff (df) CBA4 CBA1 Neocortex volume/BL2 Primates 29 12 (10) Ϫ0.613 (0.05) Ϫ0.759 (0.01) Haplorhines 22 9 (7) Ϫ0.636 (ns) Ϫ0.660 (ns) Strepsirhines 7 6 (4) Ϫ0.282 (ns) 0.771 (ns) Telencephalon/brain-stem volume Primates 29 9 (7) Ϫ0.744 (0.05) Ϫ0.663 (ns) Haplorhines 19 6 (4) Ϫ0.726 (ns) Ϫ0.643 (ns) Strepsirhines 9 7 (5) Ϫ0.760 (0.05) Ϫ0.286 (ns) duce serious problems for balancing the Strait (1999) proposed a hypothesis simi- skull on the skeleton” (Jerison, 1982, p. 82). lar to those of Hofer (1969) and Biegert In the context of such spatial constraints (1963). Noting that total basicranial length (i.e., limited cerebral diameter and tendency scales close to isometry with noncortical to sphericity), increased cerebrum size can brain volume, Strait (1999) suggested that only be accommodated by expanding the variation in the midline basicranial angle cranial base inferiorly, posteriorly, or ante- might be due to increases in the size of the riorly, thereby necessarily flexing the brain telencephalon relative to the noncortical and the basicranium. The hypothesis of part of the brain,4 rather than the size of the Jerison (1982) is refuted by animals such as brain relative to the cranial base. Analysis camels, llamas, and giraffes, which have of our data set confirms this hypothesis: long heads on relatively orthograde necks; there are significant correlations between and as discussed below, there is no convinc- flexion and the size of the telencephalon ing evidence that head and neck posture are relative to the brain stem across primates, significant influences on basicranial angle using CBA4 (Table 5). Moreover, the only in primates (Strait and Ross, 1999). significant correlation between cranial base Biegert (1963) made a claim similar to angle and a neural variable among strepsir- that of Hofer (1969), in arguing that in- rhines is the comparison of CBA4 with the creases in primate brain size relative to cra- ratio of telencephalon to brain-stem volume nial base size, as well as increases in “neo- (Table 5). However, despite relatively high pallium” (i.e., neocortex) size relative to correlation coefficients for haplorhines, these other parts of the brain, produced a rounder correlations do not remain significant with brain such that “adaptations in the struc- phylogenetically adjusted degrees of free- ture of the cranium accompanied these dom. This suggests that brain size relative changes in the size and shape of the brain” to basicranial length may be a better expla- (Biegert, 1963, p. 120). The predicted nation for flexion, because it appears to be changes in skull shape include increased more independent of phylogenetic effects. vaulting of the frontal and occipital bones Whether basicranial flexion accommo- and increased basicranial flexion. Ross and dates increases in telencephalon volume rel- Ravosa (1993) evaluated the hypothesis of ative to brain-stem volume, and/or in- Biegert (1963) by calculating correlation co- creases in overall endocranial volume efficients between cranial base angle relative to cranial base length, the end re- (CBA4) and the ratio of neocortical vol- sult is a change in brain shape. The en- 0.33 ume /basicranial length. Although they larged telencephalon of primates is an out- found a significant relationship across pri- growth of the rostral end of the brain stem mates and haplorhines, the correlation coef- that communicates with the rest of the ficients were low (around 0.5). Recalculation brain through the diencephalon at its root. of these correlation coefficients using BL2 as a measure of basicranial length produces significant correlations across primates, 4Strait (1999) refers to this as the “noncortical scaling hypoth- haplorhines, and strepsirrhines, but only esis;” however, the telencephlon consists of more than cortex: it the primate level correlations survive ad- also includes the white matter and the basal ganglia. Here we evaluate the role of relative telencephalon volume in producing justed degrees of freedom (Table 5). flexion. D.E. Lieberman et al.] PRIMATE CRANIAL BASE 137 Increasing the size of the outer cortex of the variation in cranial base angle and shape telencephalon (the neocortex) while still presented above is partially a consequence connecting to the rest of the brain through of variables other than relative encephaliza- the diencephalon might be expected to gen- tion or intrinsic brain shape. Ontogenetic erate a more spheroid shape, regardless of data are useful because they allow one to any functional constraints on skull or brain examine temporal relationships among pre- shape. In other words, the telencephalon dicted causal factors. The human ontoge- may be spheroidal because of the geometry netic data provide mixed support for the of its connections and the way it develops, hypothesis that cranial base angulation re- rather than for any functional or adaptive flects relative encephalization. Jeffery reason. Alternately, a spheroidal cerebrum (1999) found no significant relationship be- may minimize “wiring length” in the brain, tween CBA1 and IRE1 during the second a potentially important principle of design fetal trimester in humans, when brain in neural architecture (Allman and Kaas, growth is especially rapid; but Lieberman 1974; Barlow, 1986; Mitchison, 1991; Cher- and McCarthy (1999) found that the human niak, 1995; Van Essen, 1997). Accordingly, a cranial base flexes rapidly during the first 2 spheroid telencephalon may optimize neo- postnatal years, when most brain growth cortical wiring lengths as well as minimize occurs. Why relative brain size in humans the distance from all points in the cerebrum correlates with cranial base angle after to the diencephalon, a structure through birth but not before remains to be ex- which all connections to the rest of the brain plained. In addition, and in contrast to hu- must pass (Ross and Henneberg, 1995). An- mans, the cranial base in all nonhuman pri- other possible advantage of a flexed basicra- mates so far analyzed extends rather than nium derives from the in vitro experiments flexes during the period of postnatal brain of Demes (1985), showing that the angula- growth, and continues to extend throughout tion of the cranial base in combination with the period of facial growth, after brain a spherical neurocranium helps distribute growth has ceased. In Pan, for example, ap- applied stresses efficiently over a large area proximately 88% of cranial base extension and decreases stresses in the anterior cra- (CBA1) occurs after the brain has reached nial base during loading of the temporoman- 95% adult size (Lieberman and McCarthy, dibular joint. This interesting model, how- 1999). Similar results characterize other ever, requires further testing. genera (e.g., Macaca; Sirianni and Swin- Whether the spheroid shape of the tel- dler, 1985; Schneiderman, 1992). encephalon is a functional adaptation or a Ontogenetic data do not disprove the hy- structural consequence of geometry and pothesis that variation in cranial base angle developmental processes remains to be de- is related to brain size, but instead highlight termined. Nevertheless, the presence of the likelihood that the processes which gen- the cerebellum, and ultimately of the erate variation in cranial base angle are brain stem, prevents caudal expansion of polyphasic and multifactorial. Notably, the the telencephalon, making rostral expan- ontogenetic data suggest that the tight sion of the telencephalon the easiest route. structural relationship between the face This would cause the especially large hu- and the anterior cranial base (discussed be- man brain to develop a kink of the kind low) is also an important influence on cra- measured by Hofer, which in turn may nial base angle. This suggests that a large cause flexion of the basicranium. If this proportion of the interspecific variation in hypothesis is correct, then some propor- CBA, IRE, and other aspects of neural size tion of the variation in basicranial angle and shape reported above is explained by among primates is caused by intrinsic interactions between the brain and the cra- changes in brain shape, and not the rela- nial base prior to the end of the neural tionship between the size of the brain and growth phase. Thereafter, other factors (es- the base on which it sits. pecially those related to the face) influence One caution (noted above) is that ontoge- the shape of the cranial base. One obvious netic data suggest that the interspecific way to test this hypothesis is to compare the 138 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 above interspecific analyses of adults with growth, but many details of how these re- comparable analyses of infants at the period gions interact remain poorly understood. when the brain has ceased growing, but be- While the face has some influence on cranial fore much of the face has grown. base growth (see below), there are two ma- jor reasons to believe that the cranial base Brain volume and posterior cranial exerts a greater influence on the face than fossa shape vice versa during growth by setting up cer- Dean and Wood (1981, 1982) and Aiello tain key spatial relationships. First, the ma- and Dean (1990) hypothesized that in- jority of the cranial base (with the exception creases in cerebellum size correlate with in- of the ethmoidal portions of the ethmomax- creases in the size of the posterior cranial illary complex) attains adult size long before fossa. This correlation is purportedly a re- the face (Moore and Lavelle, 1974). Second, sult of increases in basicranial flexion; and as noted above, most of the face grows an- by lateral and anterior displacement of the teriorly, laterally, inferiorly, and around the lateral aspects of the petrous pyramids, cranial base. In all mammals, the upper which cause the petrous pyramids to be portion of the face (the orbital and upper more coronally oriented in humans than in nasal regions) grows antero inferiorly rela- great apes. However, Ross and Ravosa tive to the anterior cranial base and floor; (1993) found little support for a link be- and the middle face (mostly the nasal re- tween absolute cerebellum volume and gion) grows anteriorly relative to the middle CBA4; in addition, Spoor (1997) did not find cranial fossa. The lower portion of the face a correlation between cerebellum volume (the mandibular and maxillary arches and and petrous orientation. Rather, Spoor their supporting structures) interacts only (1997) showed that more coronally oriented indirectly with the cranial base, since the petrous pyramids in adult primates corre- maxillary arch grows inferiorly from the late better with increases in brain volume middle face and anteriorly relative to the relative to basicranial length. In addition, pterygoid processes of the sphenoid. the petrous pyramids, when viewed from These spatial and developmental associa- the internal aspect of the cranial base, are tions raise an important question: to what not more coronally oriented in humans vs. extent does the cranial base influence facial other apes (Spoor, 1997). growth and form? In order to address this The probable explanation for these re- issue, we first discuss the relationships be- sults may be that the posterior cranial base tween two regions of the face and cranial (Ba-S) scales with isometry against both base that are contiguous across functional cerebellum volume and the volume of infra- or developmental boundaries (the so-called tentorial neural structures (cerebellum, me- growth counterparts of Enlow, 1990): 1) the dulla oblongata, mesencephalon) (Table 4). anterior cranial fossa and the upper, orbital, If this scaling pattern characterizes those and nasal portions of the face, and 2) the dimensions of the posterior cranial fossa not middle cranial fossa and the middle, ethmo- in the mid-sagittal plane, then increased maxillary portion of the face. We conclude infratentorial neural volumes would not ne- with a brief discussion of the possible rela- cessitate changes in the proportions of the tionships between cranial base shape and entire posterior cranial fossa. This would overall facial shape. imply that variation in the orientation of Anterior cranial fossa shape and upper the petrous pyramids may be linked to facial growth changes in other cranial systems and is not solely a structural response to changes in The upper face comprises the orbital cav- cerebellar volume. ities, the orbital superstructures, and the upper portion of the nasal cavity. The upper ASSOCIATIONS BETWEEN CRANIAL face therefore incorporates elements of the BASE AND FACE anterior cranial base, including the eth- It has long been known that the cranial moid, parts of the sphenoid, and significant base plays an important role in facial portions of the frontal bone. The upper face D.E. Lieberman et al.] PRIMATE CRANIAL BASE 139 grows away from the rest of the cranial base whose orbits are closely approximated be- in three ways. Initially, as the eyeballs ex- low the olfactory tract (see also Cartmill, pand, the orbital cavity expands anteriorly, 1970, 1972; Ravosa et al., 2000a,2000b). inferiorly, and laterally through drift and Several recent studies have found support displacement (Moss and Young, 1960; En- for this hypothesis. First, brow-ridge size in low, 1990). Animals enucleated during the anthropoids (but not strepsirhines) is highly period of eyeball growth consequently have correlated with variation in the position of deficient anterior and lateral growth of the the orbits relative to the anterior cranial upper face (see Sarnat, 1982). In addition, base (Ravosa, 1988, 1991a,b; Hylander and since the roof of the orbit also contributes to Ravosa, 1992; Vinyard and Smith, 1997; the floor of the anterior cranial fossa (i.e., Lieberman, 2000; Ravosa et al., 2000b). Fi- the orbital plates of the frontal bone and nally, there is evidence that the upper face lesser wings of the sphenoid), the position, tends to be rotated dorsally relative to the orientation, and shape of the orbital roof posterior cranial base in primates with a must inevitably be affected by growth of the highly extended cranial base, but more ven- frontal lobes and anterior cranial fossa. Fi- trally rotated relative to the posterior cra- nally, the orbital cavities and superstruc- nial base in primates such as humans and tures grow anteriorly and laterally away bonobos with a more flexed cranial base (De- from the anterior cranial fossa, but only af- lattre and Fenart, 1956; Moss and Young, ter some period of postnatal development. 1960; Heintz, 1966; Cramer, 1977; Shea, In humans, for example, the upper face does 1985a, 1986, 1988; Ravosa, 1988, 1991a,b; not emerge from under the anterior cranial Lieberman, 2000). base until after the eruption of the second While the structural boundaries shared molars (Riolo et al., 1974; Lieberman, 2000). by the anterior cranial base and the upper In contrast, the front of the upper face in face result in a high degree of integration most nonhuman primates projects anteri- between these two regions, the extent to orly relative to the front of the anterior cra- which anterior cranial base shape influ- nial fossa prior to the eruption of the first ences other aspects of facial shape is less molars (Krogman, 1969; Lieberman, 1998, clear. In an interspecific study of 68 species, 2000). Variation in this spatial separation, Ross and Ravosa (1993) found that both or- termed neurocranial-orbital or neuro-or- bit and palate orientation are significantly bital disjunction, has been analyzed by var- correlated with anterior cranial base orien- ious researchers to explain ontogenetic and tation, but that palate orientation accounts interspecific patterns of supraorbital torus for none of the variation in cranial base morphology (Weidenreich, 1941; Moss and angle independent of orbital axis orienta- Young, 1960; Radinsky, 1968, 1970, 1977, tion. McCarthy and Lieberman (2001) have 1979; Shea, 1985a, 1986, 1988; Ravosa, also shown that the orientation of the orbits 1988, 1991a,b; Hylander and Ravosa, 1992; and the anterior cranial base are correlated Vinyard and Smith, 1997; Lieberman, 1998, with each other (r ϭ 0.617, P Ͻ 0.05) in 2000; Ravosa et al., 2000b). haplorhines but not in strepsirhines. These These developmental and architectural studies suggest that the orientation of the relationships between the anterior cranial anterior cranial base affects the orientation base and upper face have several conse- of the upper face directly, but that it only quences for interspecific variation in pri- indirectly influences palate orientation mates. First, the orientation of the orbits through the integration of palate and orbits and the upper face is intimately related to (see also Ravosa, 1988; Ravosa and Shea, the orientation of the anterior cranial base 1994). Consequently, it seems likely that in haplorhines (Ravosa, 1991a,b; Ross and the anterior cranial base exerts a slight in- Ravosa, 1993; Ross and Henneberg, 1995), fluence on facial orientation as a whole, but confirming the hypothesis of Dabelow (1929, that only the orbital region of the face is 1931) that the orientation of the orbits and directly integrated with the anterior cranial the anterior cranial base should be tightly base. Higher levels of integration appear to correlated in animals like haplorhines, characterize those organisms with greater 140 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

TABLE 6. Descriptive statistics for orientation of the palate relative to the anterior cranial base in primates, haplorhini, and strepsirrhini1 Planum sphenoideum Line from Sella to foramen caecum N Mean SD Minimum Maximum N Mean SD Minimum Maximum Primates 63 15.1 15.66 Ϫ41.5 45.2 60 20.0 15.15 Ϫ22.1 67.3 Haplorhines 47 12.80 16.35 Ϫ41.5 45.2 46 15.1 12.14 Ϫ22.1 52.0 Strepsirrhines 16 21.8 11.37 1.7 42.3 14 36.1 12.84 19.8 67.3 1 Calculated from data in Ross and Ravosa (1993) and Ross and Henneberg (1995), and presented above by subtracting AFK from CBA4 and CBA1. encephalization, increased orbital conver- ing the anterior-most and posterior-most as- gence, and relatively large orbits (Ravosa et pects of the cribriform plate, the mean angle al., 2000a). between these planes was 93° for cerco- Enlow (1990) proposed several structural pithecines and 86° for colobines and was relationships between the anterior cranial independent of face size. However, variabil- base and various aspects of facial shape. His ity in this angle was relatively high; and general model for the plan of the face is when the cribriform angle was measured as based almost exclusively on analyses of hu- the line connecting the anterior-most and man radiographs, and has not been care- posterior-most aspects of the cribriform fully tested in most respects. However, plate at the ethmoid/nasal cavity junction, three hypotheses are of special interest. the angle was significantly different from First, since the floor of the nasal chamber is 90° and correlated with skull size. Thus, also the roof of the oral cavity, Enlow (1990) there is only limited support for the hypoth- proposed that interorbital breadth should esis that the cribriform plate and the orien- be correlated with prognathism because tation of the snout are perpendicular. Fi- “the broad nasal base of most other mam- nally, Enlow (1990) and several others (e.g., mals supports a correspondingly much Sirianni and Swindler, 1979) have sug- longer snout.” Smith and Josell (1984) gested that the palatal plane and the ante- tested this hypothesis using a sample of 32 rior cranial base (S-FC) should be roughly primates, and found a low correlation (r ϭ parallel across primates when the cribri- 0.46) between interorbital breadth and form plate is parallel to the planum sphe- mandibular prognathism, and noted that noideum. However, interspecific analysis of the correlation was even weaker when ef- the orientation of the palate relative to both fects of overall cranial length and body size the planum sphenoideum and a line from were taken into account. This is perhaps not the sella to the foramen caecum (Table 6) surprising, as there is no obvious biome- provide little support for the hypothesis of chanical or developmental reason why the Enlow (1990) across Primates, Haplorhini, length of the face should be correlated with and Strepsirhini. the width of the posterior part of the face. Middle cranial fossa shape and Second, Enlow (1990) proposed that the ori- midfacial growth entation of the cribriform plate in all mam- mals, including primates, is perpendicular The second major region of interaction be- to the orientation of the nasomaxillary com- tween the cranial base and the face is along plex (defined as a plane from the most an- the junction between the middle cranial terior point on the frontal squama to the fossa and the posterior margins of the mid- prosthion). Ravosa and Shea (1994) investi- face. Whereas the upper face and anterior gated the angle between the cribriform cranial fossa are tightly integrated because plane (measured in two ways) and the ori- they share many of the same bony walls, the entation of the midface (measured from the middle portion of the face (the ethmomaxil- prosthion tangent to the endocranial con- lary complex) and middle cranial fossa are tour of the frontal) in a sample of Old World growth counterparts that may interact monkeys. They found that when the cribri- along their complex boundary, which lies form plane was defined as the line connect- more or less in the coronal plane (Hoyte, D.E. Lieberman et al.] PRIMATE CRANIAL BASE 141

Fig. 10. Posterior maxillary (PM) plane and 90° orientation relative to the neutral horizontal axis (NHA) of the orbits; illustrated here in, Homo sapiens. The inferior and superior termini of the PM plane are, respectively, pterygomaxillary (Ptm) and the PM point (PMp). The anterior and posterior termini of the NHA are, respectively, OM and OA (see text for definitions).

1991). In particular, the ethmomaxillary and Azuma, 1975; Enlow, 1976, 1990; En- complex grows anteriorly, laterally, and in- low and Hans, 1996), but we use here the feriorly away from the middle cranial fossa definition of Enlow and Azuma (1975), as at a number of primary growth sites (e.g., the line connecting two termini: 1) pterygo- the spheno-palatine suture, the spheno-zy- maxillary (Ptm), the average midline point gomatic suture, and the spheno-ethmoid of the most inferior and posterior points on synchondrosis). Consequently, the shape of the maxillary tuberosities; and 2) the PM the middle cranial fossa, especially the point (PMp), the average midline point of greater wings of the sphenoid (which house the anterior-most points on the lamina of the temporal lobes), must also play some the greater wings of the sphenoid (for de- role in influencing the orientation of the tails, see McCarthy and Lieberman, 2001). posterior margin of the ethmomaxillary These points and their relationship to the complex and its position relative to the rest cranial base and face are illustrated in Fig- of the cranial base. ure 10. Note that because the PM plane is Recent research on the integration of the defined using two paired registration middle cranial fossa and the midface has points, it is technically not a plane, but is focused on the role of the posterior maxil- instead an abstract line whose termini do lary (PM) plane. The PM plane has been not lie in the same parasagittal plane. De- defined in several different ways (Enlow spite its abstract nature, the PM plane is a 142 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 potentially useful analytical concept for re- searchers interested in integration between the cranial base and face because it effec- tively characterizes both the posterior mar- gin of the face and the boundary between the anterior and middle cranial fossae in lateral radiographs. The inferior terminus, Ptm, is the posterolateral corner of the eth- momaxillary complex and lies just in front of the spheno-palatine suture (Williams et al., 1995). The superior terminus, PMp, is the anterior-most point of the middle cra- nial fossa, lying close to the midpoint of the spheno-ethmoid synchondrosis and the mid- point of the spheno-frontal suture on the floor of the cranial base in all primates (Van der Linden and Enlow, 1971; McCarthy, 2001; McCarthy and Lieberman, 2001). Perhaps the most interesting aspect of the PM plane is its relationship to the orbits and the anterior cranial base. Several re- searchers have claimed that the PM plane always forms a 90° angle to the neutral hor- izontal axis (NHA) of the orbits (see Mea- surement Definitions). In their initial study, Enlow and Azuma (1975) found the PM- NHA angle to average 90° in a combined mammalian sample of 45 species, and 90° in a large sample of adult humans. Ravosa Fig. 11. Histograms comparing mean PM-NHA an- gle in samples of 18 adult anthropoid species (top) and (1991a,b), and Ravosa and Shea (1994) 15 adult strepsirrhines species (bottom). PM-NHA° is tested the PM-NHA angle in a cross-sec- not significantly different from 90° in any species. tional sample of macaques and two inter- specific sample of adult primates, and ob- tained consistent, but different PM-NHA Growth Study; n ϭ 353) aged 1 month angles from those of Enlow and Azuma through 17 years, 9 months. Also, McCarthy (1975), that ranged between 18° and 5° be- and Lieberman (in press) recently found the low 90°. However, these studies measured PM-NHA angle to average 90.0 Ϯ 0.38° SD the PM plane and the NHA (the latter only in a pooled sample of adults from 18 anthro- slightly) differently, and several more re- poid species, and 89.4 Ϯ 0.46° SD in a pooled cent studies have corroborated the original sample of adults from 15 strepsirhine spe- hypothesis of Enlow and Azuma (1975). In cies (Fig. 11). Consequently, the PM-NHA particular, Bromage (1992) found the PM- does appear to be invariant in primates, NHA angle in a cross-sectional sample of 45 with values for the most part near 90°. It Pan troglodytes crania to be 89.2 Ϯ 3.4° SD should be stressed, however, that the devel- for dental stage I, 90.5 Ϯ 3.1° SD for dental opmental and functional bases (if any) for stage II, and 88.2 Ϯ 4.0° SD for dental stage this purported invariance are still unknown III. However, these data show some signifi- and require further study. cant variation during growth, and some The 90° PM-NHA angle is useful for ex- adult crania have PM-NHA angles some- amining craniofacial integration and varia- what different from 90°, especially those for tion because, as noted above, the NHA is certain hominids. Lieberman (1998) found tightly linked to the orientation of the ante- the PM-NHA angle to be 89.9 Ϯ 1.7° SD in a rior cranial fossa and the ethmomaxillary longitudinal series of humans (Denver complex. The roofs of the orbits (which help D.E. Lieberman et al.] PRIMATE CRANIAL BASE 143 define the NHA) comprise much of the floor 1985a, 1986, 1988; Ravosa, 1988, 1991a,b; of the anterior cranial fossa. Therefore, it Ross and Ravosa, 1993; Ross, 1995a,b; May follows that the PM plane and the anterior and Sheffer, 1999; Lieberman, 2000; Ravosa cranial base should also form an approxi- et al., 2000a, 2000b). In particular, as the mately 90° angle in primates whose orbits anterior cranial base flexes relative to the are approximated to the midline. This hy- posterior cranial base, the PM plane also pothesis was tested by McCarthy and must flex relative to the posterior cranial Lieberman (2001), who found that the angle base, rotating the posterior and upper por- between the PM plane and the planum tions of the face underneath the anterior sphenoideum averaged 95.2 Ϯ 7.6° SD (n ϭ cranial fossa (klinorhynchy). In contrast, ex- 18) in anthropoids and 82.8 Ϯ 9.5° SD (n ϭ tension of the anterior cranial base relative 14) in strepsirhines. McCarthy and Lieber- to the posterior cranial base will rotate the man (2001) also found that the angle be- posterior and upper portions of the face dor- tween the PM plane and the midline ante- sally relative to the posterior cranial base rior cranial base (from the sella to the (airorhynchy) (Fig. 12). foramen caecum) averages 89.2 Ϯ 9.97° SD The relationship of the orientation of the (n ϭ 18) in anthropoids, but 70.6 Ϯ 10.5° SD back of the face (as measured for example by (n ϭ 15) in strepsirrhines. The high stan- the PM plane) to the anterior cranial base dard deviations of these angles indicate that also influences nasopharynx shape. As Fig- the integration between the back of the face ure 12 shows, flexion of the anterior cranial and the anterior cranial base is not very base and/or face relative to the posterior strong. Ross and Ravosa (1993) also came to cranial base not only rotates the face under similar conclusions by comparing the orbital the anterior cranial fossa, but it also short- axis orientation relative to the posterior cra- ens (absolutely and relatively) the length of nial base, against the orientation of the pla- the pharyngeal space between the back of num sphenoideum relative to the posterior the palate and the front of the vertebral cranial base. The differences between an- column (Laitman and Heimbuch, 1982; thropoids and strepsirhines in the relation- Spoor et al., 1999; McCarthy and Lieber- ship of the orbits to the cranial base can be man, 2001). While flexion of the cranial base explained by the fact that the roof of the during ontogeny is completely independent orbits does not contribute to the midline of the descent of the hyoid and larynx cranial base in strepsirhines, and because (Lieberman and McCarthy, 1999), variation the cribriform plate tends to be oriented in cranial base angle does influence some more vertically relative to the planum sphe- aspects of pharyngeal shape (Laitman and noideum in strepsirrhines than in anthro- Heimbuch, 1982; see below). poids (Cartmill, 1970). Ross and Henneberg (1995) suggested The potential integration of the middle that there must be functional constraints on and anterior cranial fossae with the face (as how far back the hard palate can be posi- measured via the PM plane) and the ante- tioned without occluding the airway. The rior cranial base raises several interesting integration of the anterior cranial base with issues. Most importantly, the top and back the upper and posterior margins of the face of the face appear to form an integrated means that these constraints on pharynx unit, the “facial block” which rotates during position might determine the maximum ontogeny around an axis through the inter- possible degree of basicranial angle, partic- section of the anterior and middle cranial ularly in genera such as Pongo and Alouatta fossae at the front of the greater wings of with relatively large pharyngeal structures the sphenoid (McCarthy and Lieberman, (Biegert, 1957, 1963). Ross and Henneberg 2001). This facial block is characteristic of (1995) suggested that hominoids might anthropoids but not strepsirhines, and man- have found a way to circumvent these “con- ifests itself through correlations between straints.” Hominoids have more airorhynch cranial base angle and upper facial orienta- (dorsally rotated and less frontated) orbits tion in primates (Weidenriech, 1941; Moss and palates than nonhominoid primates and Young, 1960; Biegert, 1963; Shea, with comparably flexed basicrania (Shea, 144 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

Fig. 12. Proposed “facial block,” showing the effects of angular invariance between the back of the face (summarized by the PM plane) and the top of the face, which is also the bottom of the anterior cranial base (S-FC). Changes in cranial base angle cause the top and back of the face to rotate together around an imaginary axis through the PM point. See text for details.

1985a, 1988; Ross and Henneberg, 1995). entation relative to the neurocranium, there This airorhynchy has yet to be explained is less information about the potential influ- developmentally and functionally; however, ence of the cranial base on other aspects of Ross and Henneberg (1995) suggested that facial shape such as height, length, and it evolved in hominoids in response to in- width. To what extent is overall facial shape creased flexion of the cranial base producing independent of the cranial base? It is com- posterior displacement of the palate. monly assumed that the majority of facial More research is needed on the integra- growth is independent of cranial base tion of the midface and cranial base. In par- growth, largely because much of the face ticular, why is the PM plane oriented at 90° grows in a skeletal growth trajectory after relative to the NHA during postnatal ontog- the end of the neural growth phase. In hu- eny and thus across taxa? Another question mans, for example, the face attains 95% of interest is, what aspects of cranial base adult size by 16–18 years, at least 10 years and facial shape are responsible for most of after the cranial base reaches adult size the variation in PM plane position, and (Stamrud, 1959; Moore and Lavelle, 1974). hence facial orientation? This problem has In addition, most facial and basicranial di- not been well studied, but the orientation of mensions appear to be genetically indepen- the PM plane is probably most affected by dent in adults (Cheverud, 1996). However, the size of the middle cranial fossa, espe- there is some evidence to suggest that cially the length of the temporal lobes, by changes in the proportions of the cranial flexion of the sphenoid, and by the length of base can influence facial shape. This inter- the anterior sphenoid in the midline cranial action is predicted to be especially impor- base. Three-dimensional studies of the in- tant, and perhaps exclusive to humans, in terface between the PM plane and the cra- which the upper face lies almost completely nial base are needed to resolve these and underneath the anterior cranial fossa (Wei- other questions about cranial base-face in- denreich, 1941; Howells, 1973; Enlow and terrelations and interactions. Bhatt, 1984; Enlow, 1990; Lieberman et al., 2000). Basicranial width and overall facial The most explicit of these hypotheses is shape in humans that of Enlow (1990), who suggested that Although it is clear that the cranial base humans with absolutely narrow cranial plays a major role in influencing facial ori- bases (primarily dolichocephalics) tend to D.E. Lieberman et al.] PRIMATE CRANIAL BASE 145

Fig. 13. Diagram illustrating angles and lines used from videos (see Strait and Ross, 1999, for details). The to calculate foramen magnum orientation relative to orientation of the foramen magnum relative to the or- orbital axis orientation and head-neck angle (Strait and bital axis was calculated from measures of the orienta- Ross, 1999). The orientation of the orbital aperture and tion of both these planes relative to the clivus ossis the neck inclination were measured relative to gravity occipitalis (CO) as 180°-AOA-FM Ͻ CO. have longer, more flexed cranial bases, and and face. Lieberman et al. (2000) attempted narrower faces than individuals with abso- to test the hypothesis of Enlow (1990) more lutely wider cranial bases (primarily directly with a partial correlation analysis brachycephalics). If variation in overall fa- of a sample of 98 adults from five geograph- cial size is partially independent of cranial ically and craniometrically diverse popula- base and neurocranial size, then interac- tions. The study, however, found a low cor- tions between cranial base width and facial relation between upper facial breadth and width may have some effects on facial maximum anterior cranial fossa breadth height and length. Enlow (1990) proposed (r ϭ 0.53, P Ͻ 0.001), and between midfacial that humans with absolutely narrower cra- breadth and maximum middle cranial fossa nial bases tend to have proportionately nar- breadth (r ϭ 0.49; P Ͻ 0.001) when differ- rower and antero-posteriorly longer faces ences in overall size were accounted for us- (leptoproscopy) than humans with wider ing partial correlation analysis. In addition, cranial bases, who tend to have proportion- there was only a low tendency (r ϭ 0.49, P Ͻ ately wider and antero-posteriorly shorter 0.001)5 for individuals with narrow cranial faces (euryproscopy). The hypothesis re- bases to have longer, narrower faces than ceives some support from studies of artifi- individuals with wider cranial bases, and cial cranial deformation in humans. Anto´n the trend may largely be a factor of inter- (1989, 1994), for example, showed that an- population rather than intrapopulation tero-posterior head-binding during the first variation. Further studies are needed to years of life causes not only a wider neuro- better understand these sources of varia- cranium but also a concomitantly wider face from additional growth in the most lateral regions; conversely, circumferential head- 5r ϭ 0.40, P Ͻ 0.001 when facial size is held constant (for binding results in a narrower neurocranium details, see Lieberman et al., 2000). TABLE 7. Mean values for measures of cranial base angulation, foramen magnum orientation, cranial base length, and measures of endocranial volume, including data from Ross and Ravosa (1993), Ross and Henneberg (1995), and new data collected for this study CBA41 CBA1 AOA1 AFK1 Op-Ba Ͻ clivus Basion-sella Sella-foramen Species or specimen IRE11 IRE52 (degrees) (degrees) (degrees) (degrees) (degrees)2 (mm)2 cecum (mm)2 Alouatta belzebul 0.680 0.062 186.0 183.3 192.670 175.170 116.170 23.223 36.344 Alouatta palliata 0.710 0.065 188.0 180.7 190.170 174.830 23.509 34.252 Aotus trivirgatus 0.901 0.082 180.0 176.8 168.500 147.830 126.500 11.250 21.014 Arctocebus calabarensis 0.761 0.063 168.0 194.4 175.800 157.200 128.200 13.100 17.320 Ateles fusciceps 0.916 0.085 162.0 170.3 169.500 156.660 118.830 22.593 33.015 Avahi laniger 0.824 0.068 180.0 183.7 174.830 153.170 123.500 13.625 18.224 Brachyteles arachnoides 0.883 0.083 161.0 172.5 170.400 159.400 126.500 24.024 34.352 Cacajao calvus 0.860 0.087 172.0 168.2 173.000 158.830 122.000 19.757 27.689 Callicebus moloch 0.775 0.074 176.0 176.0 164.000 156.400 131.800 15.320 19.631 Callimico goeldi 0.817 0.078 171.0 165.0 154.670 141.500 133.200 11.175 18.425 Callithrix argentata 0.771 0.074 164.0 164.8 152.000 144.330 123.830 10.443 16.929 Cebuella pygmaea 0.880 0.071 171.0 164.2 153.000 141.500 115.330 8.454 13.906 Cebus apella 0.868 0.082 173.0 166.6 165.830 154.170 123.000 20.794 27.890 Cercocebus torquatus 0.874 0.083 172.0 157.3 161.400 142.000 130.000 21.734 33.663 Cercopithecus aethiops 0.881 0.084 171.0 165.2 163.600 143.400 128.400 18.951 28.462 Cercopithecus campbelli 0.879 0.079 170.0 161.2 160.330 142.170 126.670 16.460 32.825 Cercopithecus mitis 0.832 0.080 179.0 170.0 166.170 142.830 128.830 20.226 31.501 Cheirogaleus major 0.664 181.0 186.8 176.750 154.000 108.750 13.818 Chiropotes satanas 0.850 0.085 170.0 169.5 169.830 157.833 128.000 18.543 26.481 Daubentonia madgascariensis 0.930 157.0 169.2 169.600 147.600 110.600 19.762 Erythrocebus patas 0.824 0.080 167.0 158.7 152.170 134.833 125.500 22.377 35.374 Eulemur fulvus 0.768 0.064 171.0 183.7 177.000 158.000 126.170 19.351 25.150 Euoticus elegantulus 0.827 0.065 158.0 177.7 160.500 140.830 120.500 8.989 18.417 Gorilla gorilla 1.021 0.086 148.0 157.3 163.000 150.200 124.670 43.777 48.110 Hapalemur griseus 0.795 0.064 175.0 179.5 173.170 144.170 110.600 13.809 23.179 Homo sapiens 1.635 0.118 112.0 137.5 163.330 153.500 123.670 42.751 50.598 Hylobates lar 0.918 0.084 153.0 168.3 165.500 158.333 129.334 22.265 32.856 Hylobates moloch 0.943 0.085 160.0 172.5 175.670 159.330 117.000 21.749 30.632 Indri indri 0.704 0.060 168.0 186.2 175.670 166.330 124.200 25.183 29.202 Lagothrix lagotricha 0.879 0.082 176.0 176.0 162.330 151.400 123.400 24.909 31.039 Leontopithecus rosalia 0.804 0.076 173.0 172.5 177.500 154.500 125.500 11.211 19.259 Lepilemur mustelinus 0.811 178.0 181.2 158.330 143.170 128.170 12.149 Lophocebus albigena 0.877 0.085 163.0 161.5 187.000 163.750 144.000 24.181 30.611 Loris tardigradus 0.848 0.079 162.0 187.0 152.500 119.667 117.167 10.432 13.090 Macaca nigra 0.880 0.081 158.0 151.0 154.000 134.500 122.250 22.108 32.258 Macaca sylvana 0.865 0.083 154.0 159.2 150.000 23.086 32.901 Mandrillus leucopaeus 0.842 0.079 160.0 155.0 154.600 130.600 123.000 33.170 38.816 Mandrillus sphinx 0.828 0.080 154.0 152.5 154.583 116.750 27.404 39.082 Microcebus murinus 0.820 157.0 157.830 142.833 128.000 Miopithecus talapoin 0.955 0.096 168.0 164.2 180.000 150.000 105.000 13.612 22.387 Mirza coquereli 0.666 0.057 158.0 189.0 156.670 138.167 121.167 11.991 18.179 Nasalis larvatus 0.890 158.0 188.170 161.330 129.330 Nycticebus coucang 0.747 0.065 171.0 185.5 166.830 146.330 118.670 12.933 21.012 (Continued) TABLE 7. (Continued) CBA41 CBA1 AOA1 AFK1 Op-Ba Ͻ clivus Basion-sella Sella-foramen Species or specimen IRE11 IRE52 (degrees) (degrees) (degrees) (degrees) (degrees)2 (mm)2 cecum (mm)2 Otolemur crassicaudatus 0.753 0.060 167.0 178.7 160.670 155.830 132.670 14.908 23.434 Pan troglodytes 1.039 0.091 152.0 158.7 151.670 123.000 121.830 35.633 45.114 Papio anubis 0.865 0.084 154.0 153.2 196.830 175.330 124.000 29.010 36.697 Perodicticus potto 0.731 181.0 157.500 146.333 122.834 17.820 Piliocolobus badius 0.891 0.080 156.0 166.5 176.670 161.000 115.500 21.070 30.809 Pithecia pithecia 0.771 0.074 182.0 175.8 167.400 162.000 116.000 17.670 25.883 Pongo pygmaeus 1.026 0.085 135.0 160.8 147.000 138.830 115.000 41.228 44.834 Semnopithecus entellus 0.906 0.081 148.0 159.8 150.830 145.330 122.830 21.870 33.094 Presbytis melalophos 0.917 0.087 154.0 160.7 151.830 143.500 120.670 18.318 28.798 Presbytis rubicunda 0.886 0.087 152.0 159.0 159.200 143.750 124.750 20.201 28.047 Procolobus verus 0.874 0.081 157.0 171.4 166.830 154.500 121.670 18.631 28.264 Propithecus verreauxi 0.788 0.068 168.0 184.8 148.570 137.000 117.714 20.548 25.056 Pygathrix nemaeus 0.933 0.087 145.0 156.1 151.330 143.500 120.833 20.451 30.254 Rhinopithecus roxellanae 1.002 0.089 150.0 157.2 154.500 143.830 121.340 21.601 32.294 Saguinus fuscicollis 0.769 0.075 170.0 164.5 155.670 140.000 113.500 10.395 17.039 Saimiri sciureus 0.926 0.087 169.0 165.5 153.170 135.330 118.000 12.046 20.672 Simias concolor 0.786 0.079 161.0 160.2 174.670 160.833 129.167 19.658 28.526 Symphalangus syndactylus 0.868 0.078 167.0 173.7 139.000 121.750 115.000 27.721 37.234 Tarsius syrichta 1.005 0.062 141.0 151.0 149.000 133.000 119.833 6.099 14.796 Theropithecus gelada 0.841 0.084 152.0 156.5 163.000 146.833 123.000 26.796 33.425 Trachypithecus cristata 0.857 0.076 166.0 168.0 176.170 157.500 117.670 22.247 30.804 Varecia variegata 0.752 0.062 177.0 187.8 21.726 29.495 WT 17000 0.088 156.0 OH5 0.098 135.0 Sts 5 1.292 0.100 112.5 147.0 36.700 41.700 1 Data primarily from Ross and Ravosa (1993). 2 New data collected for this study from same radiographic collection as for Ross and Ravosa (1993). 148 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 tion, and also to study potential interactions tive data. Among primates, basicranial flex- between cranial base shape and facial shape ion has been shown to be uncorrelated with in primates and other mammals. either qualitative estimates of body posture (Ross and Ravosa, 1993) or quantitative THE CRANIAL BASE AND POSTURE measures of head and neck orientation Apart from a few recent studies reviewed (Strait and Ross, 1999). The partial correla- here, little is known about the relationship tion analysis of Strait and Ross (1999) con- between basicranial morphology, head and firmed relative brain size as a more impor- neck posture, and other aspects of head tant determinant of variation in basicranial morphology related to locomotion. One per- angle, even when facial orientation and sistent hypothesis that is especially rele- head and neck posture were taken into ac- vant to hominin evolution is that flexion of count. Although foramen magnum orienta- the cranial base is an adaptation for ortho- tion relative to anterior cranial base orien- grade posture in hominins because it causes tation (S-FC) has been shown to be related the foramen magnum to have a relatively to relative brain size (Biegert, 1963; Spoor, more anterior position and ventral orienta- 1997), the relationship between head and tion (Bolk, 1909, 1910; Duckworth, 1915; neck posture and foramen magnum orienta- Weidenreich, 1941; Schultz, 1942, 1955; tion has not yet been evaluated. Ashton and Zuckerman, 1952, 1956; Ash- We gathered data on foramen magnum ton, 1952; Moore et al., 1973; Adams and orientation (FM) from the same radiographs Moore, 1975; DuBrul, 1977, 1979; Dean and used by Ross and Ravosa (1993) and Ravosa Wood, 1981, 1982). Indeed, these features (1991b), and combined these data with mea- are often invoked in attempts to reconstruct sures of hominids reported by Spoor (1993) head posture in fossil hominins (e.g., White and with measures of head and neck orien- et al., 1994). All primates have the center of tation reported by Strait and Ross (1999) mass of the head located anterior to the (Fig. 13). The head-neck angle is the angle occipital condyles, such that more anteriorly between neck inclination and orbit inclina- positioned occipital condyles relative to tion, both relative to the substrate (Strait head length reduce the lever arm between and Ross, 1999). The values for FM orienta- the center of mass and the atlanto-occipital tion relative to the clivus (FM Ͻ CO) are in joint. This balancing, in turn, reduces torque Table 7 and are summarized in Figure 14. about this joint, thereby reducing the mag- The values for FM orientation relative to nitude of the force required from the nuchal the orbital axis were calculated from mea- muscles to hold up the head (Schultz, 1942). sures of the orientation of both these planes The occipital condyles can be moved ros- relative to the clivus ossis occipitalis (CO) as trally relative to overall head length by flex- 180°-AOA-FM Ͻ CO. These data show that ing the basicranium and/or shortening the FM Ͻ CO is not significantly correlated posterior cranial base. In vitro experiments with basicranial flexion, orbital axis orien- by Demes (1985) demonstrated that the tation, the orientation of the head relative more ventral orientation of rostrally placed to the neck, or the size of the cerebellum occipital condyles orients the articular sur- relative to the posterior basicranium (Table faces closer to perpendicular to the compres- 8). Nor is foramen magnum orientation rel- sive force acting through the center of mass ative to the orbital axis (FM Ͻ AOA) corre- of the head, potentially reducing shearing lated with any of these variables, except forces acting across the joint that need to be AOA (Table 8). Of particular interest is the resisted by muscles or ligaments. lack of correlation between the head-neck There are some experimental data that angle of Strait and Ross (1999) (Fig. 14), rodents forced to walk bipedally (Moss, suggesting that foramen magnum orienta- 1961; Fenart, 1966; Riesenfeld, 1966) de- tion is not a good indicator of the orientation velop more flexed cranial bases. However, of the neck during habitual locomotion. This the hypothesis that variations in cranial calls into question attempts to estimate base angle are adaptations for head posture, head and neck posture from data on fora- however, is not well supported by compara- men magnum orientation in fossils. D.E. Lieberman et al.] PRIMATE CRANIAL BASE 149

Fig. 14. Bivariate plot of foramen magnum orientation relative to orbital axis (new data) against head-neck angle (Strait and Ross, 1999). Homo has unusually airorhynch (dorsally rotated) orbits relative to its foramen magnum orientation. Across primates the relationship between these variables is significant (r ϭ 0.541, P Ͻ 0.05); across nonhuman primates r ϭ 0.691 (P Ͻ 0.01).

TABLE 8. Pearson’s r and P-values for correlations ture. These findings suggest that the direc- between measures of foramen magnum orientation and measures of head morphology and orientation tion of gaze cannot be reoriented through evolution solely by alterations in neck ori- Ͻ Ͻ FM AOA FM CO entation or head orientation relative to the r P r P neck, and that there is a relationship be- CBA1 0.482 0.2 0.160 0.6 tween locomotor behavior and orbit orienta- CBA4 0.145 0.7 0.258 0.5 AOA 0.841 0.001* Ϫ0.378 0.3 tion relative to the rest of the skull. Head-neck angle 0.405 0.2 0.202 0.6 This latter conclusion also explains why Cerebellum/B-a-se Ϫ0.169 0.6 0.170 0.6 the orientation of the lateral semicircular * P Ͻ 0.05. canal (LSC) may correlate with head pos- ture (Fenart and Pellerin, 1988 and refer- Another widely accepted notion holds that ences therein). Humans and animals of a shift to orthogrady necessitates ventral varying postures habitually hold their flexion of the face, particularly the orbits, heads with the LSCs pitched upwards by relative to the rest of the skull so that ani- several degrees (Sakka et al., 1976; Vidal et mals can continue to look rostrally (re- al., 1986; Graf et al., 1995). The semicircu- viewed in Ross, 1995a; Strait and Ross, lar canals function as accelerometers, regis- 1999). Strait and Ross (1999) found that tering changes in head velocity (or changes most primates orient their orbits slightly therein, i.e., acceleration), not head orienta- downwards during locomotion. When other tion relative to gravity (which is accom- variables are controlled for using partial plished using the otolith organs). Thus, the correlation analysis, orbital axis orientation intrinsic function of the canals does not ex- relative to the posterior cranial base corre- plain any relationship between LSC orien- lates significantly with head and neck pos- tation and head posture. An alternative, 150 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000

Fig. 15. Bivariate plot of orbital axis orientation relative to clivus (AOA) (Ross and Henneberg, 1995) against lateral semicircular canal (LSC) orientation relative to a line from basion to nasion (Spoor, 1993). The two variables are significantly correlated across all primates (r ϭ 0.745, P Ͻ 0.01) and nonhuman primates (r ϭ 0.906, P Ͻ 0.0001). Homo has unusually airorhynch (dorsally rotated) orbits for its LSC orientation (see also Ross and Henneberg, 1995; Strait and Ross, 1999). more likely answer lies in the role of the from the annulus tendineus around the op- semicircular canals in vestibulo-ocular re- tic canal and insert on the equator of the flexes (VORs). VORs maintain a stable ret- eyeball, they lie roughly in the same trans- inal image during head movements by coor- verse plane as the orbital axis (see Measure- dinating eye movements with changes in ment Definitions). Thus, LSC orientation head velocity. To achieve this, each semicir- should be correlated with orbital axis orien- cular canal is wired up to two extraocular tation. muscles via a three-neuron reflex arc.6 Be- As an initial test of this hypothesis, Fig- cause reflex arcs are evolutionarily conser- ure 15 plots AOA (orbital axis orientation vative (Graf, 1988), each semicircular canal relative to CO) (data from Ross and Hen- must remain roughly parallel with the line neberg, 1995) against LSC orientation rela- of action of the two extraocular muscles to tive to a line from basion to sella (ba-s) which it provides primary excitatory input (Spoor and Zonneveld, 1998). Because CO is during VORs. This functional constraint very similar to the line from ba-s in most predicts that evolutionary changes in me- taxa, these two angles roughly reflect the dial and lateral rectus orientation will be orientations of the LSC and the orbital axis associated with changes in LSC orientation. both relative to the occipital clivus. Al- Because the medial and lateral recti arise though these data derive from different specimens, a significant relationship is ob- served: LSC orientation is closely correlated 6Each posterior semicircular canal is connected to its ipsilat- with orbit orientation (r ϭϪ0.824; the neg- eral superior oblique and contralateral inferior rectus, each an- terior semicircular canal to its ipsilateral superior rectus and its ative correlation reflects the fact that the contralateral inferior oblique, and each LSC to its ipsilateral LSC Ͻ ba-s angle is measured above the medial rectus and contralateral lateral rectus (Kandel et al., 1991). LSC line, while the AOA angle is measured D.E. Lieberman et al.] PRIMATE CRANIAL BASE 151 below the orbital axis line). These data mates were nocturnal visual predators of therefore lend support to the hypothesis small invertebrates and vertebrates, and that animals orient their heads at rest (and this required more anteriorly facing and during locomotion) primarily to orient their closely approximated orbital apertures eyes towards the horizon rather than to ori- (Cartmill, 1970, 1972, 1974, 1992). In- ent their semicircular canals in any partic- creased orbital convergence enlarges the ular way. In sum, orbital axis orientation binocular field for greater stereoscopic vi- relative to the clivus and foramen magnum sion and a clear retinal image for depth orientation relative to the orbital axis are perception and prey location (Allman, 1977, hypothesized to be evolutionary adaptations 1982). The VPH further posits that rela- to head posture during habitual locomotion, tively larger orbits and grasping append- and appear necessary because of the limited ages with nails are adaptations to being range of motion at the atlanto-occipital joint nocturnal in an arboreal, terminal-branch (Graf et al., 1995). setting (Cartmill, 1970, 1972, 1974, 1992; MAJOR UNRESOLVED ISSUES OF Kay and Cartmill, 1974, 1977; Dagosto, CRANIAL BASE VARIATION IN PRIMATE 1988; Covert and Hamrick, 1993; Hamrick, EVOLUTION 1998, 1999; Lemelin, 1999). These adapta- tions differ significantly from the cranial Studies of cranial base variation in fossil and locomotor specializations of putative primates and hominins have been rare be- sister taxa such as plesiadapiforms and der- cause this region of the skull is usually mopterans (Cartmill, 1972, 1974, 1992; Kay poorly preserved or destroyed in most fos- and Cartmill, 1974, 1977; Beard, 1993; Ra- sils, and because it is hard to visualize or vosa et al., 2000a). measure without radiographs or computed According to the VPH, increased orbital tomography (CT) scans. The coming years, convergence moves the orbital apertures out however, are likely to see a renaissance of of the plane of the temporal fossa, a condi- research on the role of the cranial base in tion entailing greater ocular disruption dur- primate cranial evolution as CT scans of ing mastication (Cartmill, 1970, 1972, 1974, fossils become more readily available. Here 1992). A rigid postorbital bar may function we review six major topics where future re- search on the cranial base in both fossil and to stiffen the lateral orbital margins and extant primates promises to provide impor- thus counter ocular deformation during bit- tant insights: 1) the relationship between ing and chewing to ensure a high level of encephalization, circumorbital form, and stereoscopic acuity in an organism that pro- the origin of primates; 2) the evolution of cesses food while hunting and foraging the integrated “facial block” in haplorhines; (Cartmill, 1970, 1972). This appears to be 3) the determinants of basicranial flexion in particularly important, given that strep- hominins; 4) the relationship between basi- sirhines with unfused symphyses have been cranial flexion and the shape of the vocal shown to recruit relatively less balancing- tract; 5) the role of the cranial base in facial side than working-side adductor muscle retraction in Homo sapiens; and 6) the reli- force during unilateral mastication (Hy- ability of basicranial characters as indica- lander et al., 1998, 2000). This differential tors of primate phylogeny. muscle recruitment results in a pattern of lower strains along the balancing-side pos- Primate origins, encephalization, and torbital bar than the working-side postor- circumorbital form bital bar (Ravosa et al., 2000a). Thus, an The basicranium likely played a key role organism with a postorbital ligament and a in the evolution of the unique configuration stepsirhine-like adductor pattern (the latter of the primate skull. Over the past three of which is inferred for basal primates based decades, the visual predation hypothesis on the presence of unfused symphyses; Ra- (VPH) has become a well-accepted model of vosa, 1996, 1999) would experience an primate origins (Martin, 1990; Fleagle, asymmetrical circumorbital and, in turn, an 1999). The VPH argues that the first pri- ocular loading pattern that is hypothesized 152 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 to compromise effective stereoscopic visual 2000a). This combination of derived fea- acuity. tures creates a spatial packing problem in Analyses of felids (perhaps the best ana- which the position of the frontal lobes and log for the skull of basal primates), herpes- anterior cranial fossa have a major influ- tids, and pteropodids demonstrate that ence on orbital aperture orientation, inte- postorbital bar formation characterizes taxa grating morphological variation in these ad- with increased orbital convergence and/or jacent cranial regions (see above). Because greater orbital frontation (Noble et al., neural and ocular size scale with negative 2000; Ravosa et al., 2000a). As both orbital allometry (Schultz, 1940; Gould, 1975), this characteristics became more developed dur- structural constraint would be particularly ing early primate evolution (Simons, 1962; marked in smaller, and thus more fron- Cartmill, 1970, 1972, 1974, 1992; Szalay et tated, taxa—the morphospace in which al., 1987; Martin, 1990; Fleagle, 1999), it is basal primates and felids happen to develop likely that primate postorbital bar develop- postorbital bars. ment is correlated with both evolutionary Anthropoid origins and cranial transformations in the orbital complex (Ra- base-face interactions vosa et al., 2000a). The role of orbital frontation in postor- Another interesting problem is the role of bital bar formation is especially significant the cranial base in the fundamental rear- because it apparently reflects interactions rangement of the face along the stem lin- among several factors unique to the early eage leading to haplorhines and anthro- evolution of small primates (Ravosa et al., poids. These changes include: increased 2000a). First among these factors is enceph- orbital convergence and frontation; in- alization. Both early primates and their pu- creased relative brain size, especially in the tative ancestors were tiny, weighing be- frontal and temporal lobes; a more acutely tween 100–300 g (Kay and Cartmill, 1977; angled (flexed) cranial base; partial retrac- Dagosto, 1988; Martin, 1990; Beard, 1993; tion of the face below the braincase; re- Covert and Hamrick, 1993; Fleagle, 1999). duction of the olfactory apparatus and Thus, the greater encephalization of basal interorbital region with concomitant primates (Martin, 1990) did not result from approximation of the orbits; relatively phyletic size decreases7 (Gould, 1975; Shea, smaller orbits associated with diurnality; 1987). Instead, increased relative brain size and the presence of a postorbital septum and orbital frontation appear linked to noc- (Cartmill, 1970, 1980; Radinsky, 1968, turnal visual predation (Ravosa et al., 1979; Rosenberger, 1985, 1986; Ravosa, 2000a), which is related to increases in the 1991b; Ross and Ravosa, 1993; Ross, relative size of the visual cortex (Cartmill, 1995a,b). Not surprisingly, changes in cra- 1974, 1992) and greater encephalization nial base shape have been key features of all (Barton, 1998). This hypothesis comple- the models proposed to explain the order in ments prior claims that increased enceph- which these features arose, their putative alization in basal primates is related to the functions, and their interactions. According unique combination of arboreality, precoci- to Cartmill (1970), the fundamental differ- ality, and small body size (Shea, 1987). ence between haplorhines and strepsirhines Apart from being more encephalized than centers on whether orbital convergence oc- nonprimate archontans, the first primates curs towards the top of the skull or at the (and felids) possessed relatively larger eyes front. If, as in haplorhines, the orbits con- and more convergent orbits (Kay and Cart- verge anteriorly (associated with increased mill, 1977; Martin, 1990; Covert and Ham- orbital frontation), then the orbits not only rick, 1993; Cartmill, 1992; Ravosa et al., compress the olfactory region, reducing its dimensions, but also become closely approx- imated to the midline anterior cranial base. 7As phyletic dwarfs are more encephalized than like-sized This necessarily reduces the size of the ol- sister taxa (Gould, 1975; Shea, 1987), presumably they are also factory apparatus and forms an interorbital more flexed, highlighting the complex relationships between brain evolution and changes in basicranial and facial form. septum, facilitating a subsequent increase D.E. Lieberman et al.] PRIMATE CRANIAL BASE 153 in relative encephalization by expansion of Variation in hominin cranial base angle the brain forward over the top of the orbits. How to account for variation in basicra- It has been argued that, as predicted by nial flexion in hominins has been controver- Dabelow (1931), by bringing the orbits and sial and remains unresolved. Several recent anterior cranial base into close continuity, studies (e.g., Ross and Henneberg, 1995; they became structurally integrated such Spoor, 1997) have shown that the cranial that changes in the orientation of one nec- base in Australopithecus and Homo is gen- essarily affect the other (Ross and Ravosa, erally more flexed than in Pan or other non- 1993). Small nocturnal strepsirhines, in human primates. This difference raises two contrast, tend to converge their orbits to- questions. First, how much is cranial base wards the top of their head, not compressing the olfactory apparatus, and preventing flexion among early hominins related to up- brain expansion over the orbits concomitant right posture, facial orientation, or brain with a shift to diurnality. The orbits and size? Second, what factors account for the anterior cranial base in all strepsirhines are observed variation in cranial base angle not as unified structurally, and thus basi- among hominins? cranial flexion and orbit orientation do not Although cranial base angles vary sub- covary as greatly. stantially among hominin species, australo- The evidence that all omomyiforms that pithecines have CBAs generally intermedi- are well enough preserved have an interor- ate between humans and chimpanzees, but bital septum below the olfactory tract, like with more flexed cranial bases among A. that of Tarsius and small anthropoids (Ross, boisei and less flexed cranial bases for A. 1994), suggests that this integration of an- aethiopicus (KNM-WT 17000) (F. Spoor, terior cranial base and upper face may be an personal communication). Until now, the early unique derived feature of the haplo- hypothesis that cranial base flexion in homi- rhine stem lineage. This integration set the nins is an adaptation for increased brain stage for the subsequent evolution of the size relative to basicranial length (Gould, haplorhine postorbital septum. Increased 1977) has received the most support (Ross orbital frontation (klinorhynchy) and con- and Ravosa, 1993; Ross and Henneberg, vergence in early anthropoids caused the 1995; Spoor, 1997; McCarthy, 2001). In par- anterior temporal muscles and orbit to come ticular, if one measures IRE5 vs. CBA1 into close proximity, leading to the evolution (thereby including the cribriform plate in of a postorbital septum (Ross, 1995b, 1996). measures of both basicranial length and the Exactly why increased frontation occurred angle of the cranial base), then H. sapiens in haplorhines remains unexplained, al- and other hominin taxa such as A. africanus though it has been argued that increased have exactly the degree of flexion expected relative brain size might have caused in- by basicranial length. creased basicranial flexion, producing in- However, not all of the variation in homi- creased orbital frontation as a consequence nin CBA can be explained by relative brain of the integration of the anterior cranial size. For example, Neanderthals and ar- base and orbits (Ross, 1996; see also Ravosa chaic Homo fossils such as Kabwe have con- et al., 2000a on the effects of small size on siderably more extended CBA1s than H. sa- skull form in basal primates). This hypoth- piens (about 15°), even though they are esis remains to be evaluated in fossil stem bipedal and similarly encephalized (Ruff et anthropoids for want of well-preserved spec- al., 1997). In addition, other measures of imens, but is not supported by the fact that cranial base angle and relative encephaliza- early anthropoids had a postorbital septum tion, which do not include the cribriform in conjunction with relatively small brains plate (CBA4 and IRE5), indicate that H. (Ross, 2000). It remains to be determined sapiens have less flexed cranial bases then why the haplorhine stem lineage evolved expected for anthropoids of their size (Ross more frontated orbits, but the findings of and Henneberg, 1995). This finding high- Strait and Ross (1999) suggest that the role lights the likelihood that no single explana- of posture should be considered. tion will account for interspecific differences 154 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 in CBA among hominins. Other factors that tions to produce a wide range of vowels have been argued to contribute to variation whose formant frequencies are acoustically in CBA, including facial kyphosis and head distinct regardless of vocal tract length and neck posture, cannot be shown to be (Fant, 1960; Nearey, 1978; Lieberman, important correlates of basicranial flexion. 1984; Carre et al., 1994; Beckman et al., Most importantly, the comparative study by 1995). Strait and Ross (1999) of CBA, head-neck Although the speech-related acoustical angle, and orbital axis orientation among properties of the unique human vocal tract extant primates found that basicranial flex- are not in dispute, the role of cranial base ion is primarily influenced by relative brain flexion in hyo-laryngeal descent is contro- size and not head and neck posture. The versial, yet potentially important for recon- traditional view that human basicranial structing the anatomy of the vocal tract in flexion is somehow an adaptation for ortho- fossil hominins Two questions are of special grade posture is no longer tenable. importance. First, what is the relationship of external cranial base flexion to the de- Cranial base flexion and vocal tract scent and/or positioning of the hyoid rela- shape in hominins tive to the oral cavity? Second, how does the Flexion of the cranial base has been ar- angle of the external cranial base change gued to be an important correlate of the during development, and what is its rela- shape of the vocal tract. In particular, sev- tionship to internal cranial base angle? eral researchers (Lieberman et al., 1972, The original hypothesis that flexion of the 1992; Laitman and Crelin, 1976; Laitman et external cranial base in humans contributes al., 1978, 1979; Laitman and Heimbuch, to laryngeal descent, and thus can be used 1982) claimed that the degree of flexion of to reconstruct the vocal tract of fossil homi- the external cranial base (between the infe- nins (Lieberman and Crelin, 1971; Lieber- rior aspect of the basioccipital clivus and the man et al., 1972; Laitman and Crelin, 1976; palate) influences the position of the hyo- Laitman and Heimbuch, 1982; Lieberman, laryngeal complex. In most mammals, the 1984), was based on three observations. hyoid and larynx lie close to the soft palate First, these researchers inferred a relation- so that the epiglottis and soft palate can ship between cranial base flexion and laryn- engage, permitting simultaneous breathing geal descent on the basis of comparisons of and swallowing (Laitman and Reidenberg, neonatal and adult humans vs. nonhuman 1993; German et al., 1996; Larson and Her- primates. In particular, human neonates, ring, 1996; Crompton et al., 1997). In con- like nonhuman primate adults, have a rela- trast, humans have a uniquely shaped phar- tively extended cranial base and a high hy- ynx in which the hyo-laryngeal complex oid, whereas only human adults have both a descends inferiorly relative to the oral cav- flexed cranial base and a descended larynx. ity, causing the soft palate and epiglottis to Second, internal and external basicranial become disengaged so that the trachea and flexion were believed to covary with the de- esophagus share a common passageway scent of the larynx (George, 1978). Third, (Negus, 1949; Crelin, 1973). Hyo-laryngeal external cranial base flexion was believed to descent is an important physiological basis reorient the suprahyoid muscles and liga- for many aspects of human speech. Flexion ments more vertically, and to shorten the of the external cranial base in combination antero-posterior length of the oropharynx with a low position of the larynx relative to between the palate and the cervical verte- the palate divide the human vocal tract (VT) brae, thus requiring the larynx and poste- into separate horizontal and vertical “tubes” rior tongue to be positioned lower relative to of approximately equal length, whose cross- the hard palate. sectional areas can be modified indepen- Lieberman and McCarthy (1999) tested dently at least tenfold by the tongue the relationship between cranial base flex- (Stevens and House, 1955; Fant, 1960; ion and hyo-laryngeal position using a lon- Stevens, 1972; Baer et al., 1991). Dynamic gitudinal series of radiographs in humans filtering in the two-tube human VT func- (the Denver Growth Study), which pre- D.E. Lieberman et al.] PRIMATE CRANIAL BASE 155

Fig. 16. Longitudinal changes in the angle of the 13 females (for details, see Lieberman and McCarthy, external cranial base (CBA5 from basion-sphenobasion- 1999). Note that the height of the vocal tract continues hormion) and the height of the vocal tract (the distance to grow throughout the somatic growth period, whereas from the vocal folds to the plane of the hard palate, the external cranial base angle ceases to change appre- perpendicular to the posterior pharyngeal wall). Data ciably after approximately 3 postnatal years. are from a longitudinal study of growth in 15 males and served details of larynx and hyoid position External flexion has been measured in in upright subjects x-rayed during quiet res- several ways, all of which suggest that ex- piration. This study found no statistically ternal and internal cranial base angles are significant relationship between either in- correlated with each other, but differ in ternal or external cranial base flexion and their pattern of growth in humans and non- hyo-laryngeal descent. As Figure 16 shows, human primates. Laitman et al. (1976, the cranial base and the position of the lar- 1978, 1979, 1982) developed a composite, ynx must be partially independent in hu- size-corrected measure of exocranial flexion mans because the cranial base flexes rapidly between the basioccipital and the palate, during the first few years after birth, which they measured on cross-sectional whereas the larynx and hyoid descend grad- samples of humans, apes, monkeys, and ually until the end of the adolescent growth several fossil hominins. More recently, spurt. Consequently, the flexion of the ex- Lieberman and McCarthy (1999) measured ternal cranial base (and presumably its ef- external cranial base flexion in a longitudi- fects on suprahyoid muscle orientation) can- nal sample of humans using two lines, one not be used to infer vocal tract dimensions extending from basion to sphenobasion, and in fossil hominins (Lieberman et al., 1998). the second from sphenobasion to hormion. Similarly, Chan (1991) demonstrated that May and Sheffer (1999) took essentially the the correlation between styloid process ori- same measurement on cross-sectional sam- entation and laryngeal position is not strong ples of humans, chimpanzees, gorillas, and enough to estimate vocal tract dimensions several fossil hominins. These studies all reliably. agree that flexion of the internal cranial 156 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 base in humans occurs prior to the eruption 1997; May and Sheffer, 1999; Ravosa et al., of the first permanent molars and then re- 2000b). As a consequence, H. sapiens also mains stable, but that the external cranial has a more vertical frontal profile, less pro- base extends gradually in all nonhuman pri- jecting browridges, a rounder overall cra- mates throughout the period of facial nial shape, and a relatively shorter oropha- growth.8 Moreover, the patterns of external ryngeal space between the back of the hard and internal cranial base angulation mirror palate and the foramen magnum—virtually each other. The internal cranial base (mea- all of the supposed autapomorphies of “an- sured using both Ba-S-FC and Landzert’s atomically modern” H. sapiens. angle) flexes in humans rapidly prior to 2 What is the role of the cranial base in postnatal years and then remains stable, facial projection? Lieberman (1998, 2000) but extends in nonhuman primates gradu- proposed that four independent factors ac- ally throughout the period of facial growth count for variation in facial projection: 1) (Fig. 7) (Lieberman and McCarthy, 1999). antero-posterior facial length, 2) anterior cranial base length, 3) cranial base angle, Cranial base shape and facial and 4) the antero-posterior length of the projection in Homo middle cranial fossa from sella to PM Although the effects of cranial base angu- plane.9 Each of these variables has a differ- lation on the angle of the face relative to the ent growth pattern, but combine to influ- rest of the skull (facial kyphosis) have long ence the position of the face relative to the been the subject of much research (see basicranium and neurocranium. For exam- above), there has been recent interest in the ple, facial projection can occur through hav- role of the cranial base on facial projection. ing a long face relative to a short anterior Facial projection (which is a more general cranial fossa, a long middle cranial fossa term for neuro-orbital disjunction) is de- relative to the length of the anterior cranial fined here as the extent to which the nonros- fossa, and/or a more extended cranial base. tral portion of the face is positioned anteri- Partial correlation analyses of cross-sec- orly relative to the foramen caecum, the tional samples of Homo sapiens and Pan most antero-inferior point on the cranial troglodytes indicate that each contributes base (note that facial projection and prog- significantly to the ontogeny of facial projec- nathism are different). Variation in facial tion in humans and apes when the associa- projection, along with an understanding of tions between these variables and with their developmental bases, may be impor- overall cranial length and endocranial vol- tant for testing hypotheses about recent ume as well as other cranial dimensions are hominin evolution. In particular, Lieber- held constant (Lieberman, 2000). In other man (1995, 1998, 2000) has argued that words, chimpanzees and humans with rela- variation in facial projection accounts for tively longer faces, shorter anterior cranial many of the major differences in overall bases, less flexed cranial bases, and/or craniofacial form between H. sapiens and longer middle cranial fossae tend to have other closely-related “archaic” Homo taxa, relatively more projecting faces. including the Neanderthals. Whereas all In an analysis of radiographs of fossil nonextant hominins have projecting faces, hominins, Lieberman (1998) argued that “anatomically modern” H. sapiens is the major cause for facial retraction and its uniquely characterized by a retracted facial resulting effects on modern human cranial profile in which the majority of the face lies shape was a change in the cranial base beneath the braincase (Weidenreich, 1941; rather than the face itself. Specifically, mid- Moss and Young, 1960; Vinyard, 1994; dle cranial fossa length (termed ASL) was Lieberman, 1995, 1998; Vinyard and Smith, estimated to be approximately 25% shorter in anatomically modern humans, both re-

8May and Sheffer (1999) did not find evidence for postnatal extension of the cranial base in Pan, largely because of insuffi- 9This dimension was originally termed anterior sphenoid cient sample sizes that were divided into overly large ontoge- length (ASL), but it is really a measure of the midline prechordal netic stages. length of the middle cranial fossa (Lieberman, 2000). D.E. Lieberman et al.] PRIMATE CRANIAL BASE 157

Fig. 17. Thin-plate spline analysis of an Australian male (from Queensland) relative to Kabwe 1 (target). Eighteen landmarks from each skull were initially superimposed using a resistant-fit Procrustes analysis. The deformation grid shows that the archaic Homo fossil has a relatively more projecting and taller face, a more extended cranial base, a relatively shorter middle cranial fossa, and a relatively longer pharyngeal space between the palate and the foramen magnum. cent and Pleistocene, than in Neanderthals (P Ͻ 0.05). Consequently, Spoor et al. (1999) and other taxa of archaic Homo, whereas and Lieberman (2000) concluded that differ- anterior cranial base length and facial ences in cranial base angle are more likely length were not significantly different be- to account for facial retraction in modern tween these taxa. humans, as well as for other differences Lieberman (1998), however, incorrectly noted by Lieberman (1998), such as the rel- measured ASL in the few archaic humans in atively shorter pharynx behind the palate. which the cranial base is well preserved. As This hypothesis needs to be tested carefully, shown by Spoor et al. (1999), ASL is not but is explored here in a preliminary fash- significantly longer in archaic Homo than in ion with a geometric morphometric analysis modern humans, but the angle of the cra- comparing the shape of the Kabwe cranium nial base (CBA1) is about 15° more extended with a large, robust recent H. sapiens (a in archaic Homo fossils such as Gibraltar, male Australian). Figure 17 shows a thin- Monte Circeo, and Kabwe than in samples plate spline transformation of the Austra- of Pleistocene and recent modern humans lian into Kabwe (computed using Mor- 158 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 phometrika, version 0.007, Jeff Walker, Ma and Lozanoff, 1999). The extent to Chicago, IL), based on an initial resistant-fit which the morphological differences be- superimposition Procrustes analysis of six tween the retrognathic Br mouse and con- cranial base landmarks, seven facial land- trols is at all similar to the differences evi- marks, and five neurocranial landmarks.10 dent between H. sapiens and archaic Homo The thin-plate spline, which is based on a has yet to be determined. However, these Procrustes analysis that geometrically cor- studies, in conjunction with facial growth rects for most effects of size differences, defects caused by chondrogenic growth dis- shows that Kabwe has a considerably more orders such as Crouzon syndrome, Pierre- projecting face (i.e., between nasion and the Robin syndrome, and Down syndrome, high- foramen caecum) in conjunction with a rel- light the important role the cranial base atively more extended cranial base (14o), a plays in facial growth and integration (Dav- dorsally rotated PM plane relative to the id et al., 1989). posterior cranial base, and a relatively Cranial base characters in phylogenetic longer pharyngeal space between the max- analyses illa and the foramen magnum. In addition, when one examines specific, size-corrected One final consideration of interest is dimensions (standardized by the geometric whether it might be profitable to focus on mean of all the interlandmark distances), characters from the cranial base in taxo- midfacial length (PM-Na) is 19% longer in nomic and phylogenetic analyses of pri- Kabwe than in the Australian modern indi- mates. This possibility has been raised by a vidual, but the length of the anterior cranial number of authors (e.g., Olson, 1985; Shea, base (S-FC) is only 4% shorter. In other 1985a, 1988; Lieberman et al., 1996; Lieber- words, Kabwe exhibits a considerably more man, 1997; Strait et al., 1997; Strait, 1998) projecting face than the H. sapiens speci- for three reasons. First, the cranial base men because it has a more extended cranial derives from endochrondral precursors base in conjunction with a relatively longer rather than though intramembranous ossi- face. Changes in middle cranial fossa shape, fication processes (endochondral bones are therefore, appear to have had major effects thought to have more direct genetic influ- on facial retraction in human evolution, but ence in terms of initial shape); second, the need to be further examined using addi- cranial base is the first part of the skull to tional specimens. reach adult size and shape (Moore and Additional, intriguing evidence that the Lavelle, 1974); and third, the cranial base cranial base can play an important role in may play a greater role in influencing facial facial retraction may be come from studies shape than vice versa (see above). Conse- of craniofacial growth abnormalities and quently, one might expect cranial base char- from laboratory studies of mice. Mice that acters to preserve more phylogenetic signal are homozygous-recessive for the retrog- than facial characters by virtue of being nathic Brachyrrhine (Br) allele are charac- more heritable and less influenced by the terized by a primary growth defect in the epigenetic responses to external influences anterior cranial base (Beechey et al., 1998; during postnatal ontogeny rampant in the Ma and Lozanoff, 1999) that leads to a se- facial skeleton (Herring, 1993). verely retrognathic midfacial profile but a Expectations aside, there are currently no morphologically normal nasal septum and data suggesting that the basicranium is ac- face (Lozanoff, 1993; Lozanoff et al., 1994; tually a better source of characters than other regions of the skull for phylogenetic analyses. In terms of narrow-sense herita- bility (h2), basicranial, neurocranial, and fa- 10These landmarks are: basion, sella, pituitary point, sphenoi- dale, PMp (the anteriormost point on the greater wings of the cial characters have similar levels of herita- sphenoid), foramen caecum, nasion, ANS, PNS, prosthion, max- bility among primates (Sjøvold, 1984; illary tuberosities, fronton, orbitale, opisthocranion, the superi- or-most point on the vault, fronton, the inferior-most point on Cheverud and Buikstra, 1982; Cheverud, the supratoral sulcus, glabella. Resistant fit superimposition 1995). In addition, basicranial variables ap- was used in order to minimize effects of the very different shape of the neurocranium in archaic Homo vs. modern H. sapiens. pear to be equally well (or poorly) correlated D.E. Lieberman et al.] PRIMATE CRANIAL BASE 159 with other dimensions or features in homi- on the results has yet to be determined. noids (Strait, 1998), and in the human skull Further study of these interactions is (Lieberman et al., 2000). Finally, those few needed to improve the reliability of phyloge- studies that have focused on cranial base netic analyses, and again highlight the need characters do not yield results substantially to consider morphological characters in different from analyses that incorporate terms of their generative processes (e.g., other craniodental characters. Lieberman et Gould, 1977; Cheverud, 1982; Shea, 1985b; al. (1996) found that basicranial and vault Hall, 1994; Lieberman, 1999). characters tend to yield similar cladograms CONCLUSIONS that differ only slightly from cladograms based on facial characters. Strait et al. Since the last major reviews of cranial (1997) did not specifically examine charac- base anatomy in primates (Scott, 1958; ters from the cranial base, but found no Moore and Lavelle, 1974; Sirianni and major difference between trees based on Swindler, 1979), there has been a tremen- masticatory characters vs. those that were dous increase in our knowledge of chondro- predominantly neurocranial and basicra- cranial embryology, the patterns and pro- nial. In their study of primate higher taxo- cesses of basicranial growth, and the nature nomic relationships, Ross et al. (1998) found of basicranial variation across primates. the cranial data, consisting primarily of ba- Major advances include details of the mor- sicranial traits, to yield trees similar to phogenetic independence between the pre- those produced by the dental data, although chordal and postchordal portions of the with better resolution at older nodes. Thus, chondrocranium; comparative data on the whether the basicranium is a better source relative importance of brain size, orbital ori- of phylogenetic data remains open to ques- entation, facial orientation, and posture as tion. The cranial base may be a good place to factors that account for variation in cranial look for reliable characters if researchers base angulation; and ontogenetic and com- are to focus on characters that describe de- parative data on the structural relation- velopmental processes or events (e.g., flex- ships between the anterior cranial base and ion vs. extension at the spheno-occipital upper face in haplorhines vs. strepsirhines, synchondrosis) rather than using charac- and their influences on facial form. Despite ters that solely describe morphological vari- these advances, many aspects of cranial ation (e.g., the angle of the whole cranial base growth, variation, and function remain base) (Hall, 1994; Lieberman, 1999). This poorly understood. For example, we do not hypothesis, however, has yet to be tested. know what ontogenetic processes govern The above studies, however, raise another flexion and extension of the cranial base, or key issue relevant to phylogenetic studies: which synchondroses are active in cranial the problem of independence. Cladistic base elongation vs. angulation in humans analyses explicitly require one to use inde- and other primates. Future research needs pendent characters to avoid problems of to be aimed at studying these processes as convergent and correlated characters incor- they relate to cranial shape, function, and rectly biasing the outcome of any parsimony evolution. analysis. Yet the above studies demonstrate To conclude, we highlight two important the existence of multiple and complicated practical and theoretical issues which we interactions between the cranial base and believe merit special consideration, and the neurocranium and between the cranial which promise to further our understanding base and the face. For example, variations of craniofacial growth and variation. First, in orbit size and orientation are linked to what are the major factors that generate variations in the angle of the cranial base, variation in the cranial base among pri- brain size, and the orientation of the face mates? Second, to what extent does the cra- relative to the rest of the skull. Many of nial base function to coordinate these fac- these features have been treated as inde- tors within the craniofacial complex during pendent characters in recent cladistic anal- growth and development? As noted above, yses (e.g., Strait et al, 1997), but their effect these questions need to be addressed using 160 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 two approaches. Ontogenetic studies are (see also Olson and Miller, 1958; Cheverud, crucial for testing hypotheses about the gen- 1982; Zelditch, 1988),11 is an important is- eration of morphological covariation pat- sue because of the many genetic, develop- terns, and comparative studies are impor- mental, and functional interactions that oc- tant for probing the extent to which cur between the basicranium and its interspecific patterns of morphological evo- neighboring anatomical components. As de- lution are epiphenomena of developmental scribed above, the cranial base is likely to processes. directly interact, developmentally and func- tionally, with various adjoining skeletal, What major factors generate variation muscular, and neurosensory complexes, in the cranial base? most notably the brain, the orbits, the eth- The studies summarized above suggest momaxillary complex, and the neck. These that relative brain size, particularly relative “units,” in turn, have direct and indirect to basicranial length, is an important deter- interactions with other putative units such minant of the degree of basicranial angula- as the oropharynx, nasopharynx, mandible, tion. However, the effects of (especially and maxillary arches. prenatal) brain shape on basicranial But does the cranial base play an active or morphology have yet to be thoroughly inves- a passive role in integrating cranial shape tigated. Further experimental and compar- among these disparate units, and how much ative morphological research is needed to integration actually occurs? On an intuitive relate soft-tissue and bony morphology in level, there are several reasons to suggest the primate head. Despite a long tradition that the cranial base acts in part as a struc- suggesting links between basicranial mor- tural “interface” during growth between the phology and head, neck, or body posture, brain and the face, and between the head there is currently little empirical support and the neck. In many regions, the basicra- for the hypothesis that these factors are di- nium serves as the actual structural bound- rectly related to variation in the cranial ary between disparate components of the base, especially angulation in the midsagit- skull: the floor of the anterior cranial fossa tal plane. Better data are also needed on is the roof of the orbits; the back of the head and neck posture during locomotion midface is the front of the middle cranial before locomotor-related cranial adapta- fossa; and the posterior cranial base is the tions can be definitively identified. How- posterior roof of the oropharynx. Yet, in ever, connections between facial orientation spite of these obvious relationships, it is and basicranial morphology on the one hand difficult to define or assess quantitative hy- and head posture on the other leave open potheses about craniofacial integration be- the possibility of an indirect link between cause we know so little about the extent and basicranial angle and head posture. nature of the numerous interactions that presumably occur between and among re- What role does the cranial base play in gions of the cranial base and other parts of craniofacial integration? the skull. What are the actual units in the Because many variables influence cranial cranial base and skull that interact, and base shape, it follows that these variables what regulates their interrelations and, es- also influence other aspects of cranial shape pecially, interactions? In other words, the via the cranial base. Consequently, a key appropriate null hypothesis to be tested is issue that emerges repeatedly in discus- that the cranial base, while associated with sions of the role of the basicranium in cra- variation in other parts of the skull, plays nial development, growth, and evolution is integration. Integration, which is defined here as “the association of elements through 11Note that some researchers (most notably Olson and Miller, a set of causal mechanisms so that change 1958) define morphological integration solely as a multivariate pattern of covariation with regard to some a priori biological in one element is reflected by change in hypothesis (thus recognizing the importance of generative pro- another” (Smith, 1996, p. 70), thereby gen- cesses), whereas others (e.g., Cheverud, 1996) define integration more generally as either a pattern or a process that refers to erating a pattern of significant covariation “connections or relationships among morphological elements.” D.E. Lieberman et al.] PRIMATE CRANIAL BASE 161 no more of an integrative role than any liminary fashion to solely phenotypic varia- other part of the skull (e.g., the mandible, tion in the cranial base, using the data the brain). presented above. In order to explore the basicranium’s role in craniofacial integration, it is first neces- Correlation. Integration is most basi- sary to decide how to test hypotheses about cally revealed by complex patterns of corre- the many different processes through which lation and covariation which indicate a lack integration occurs, and the many structural of independence among variables (see Chev- and functional levels at which integration is erud, 1995, 1996), and which can be recog- evident. Readers interested in this huge and nized a posteriori by comparing theoreti- complex topic (which is too large to review cally and empirically derived correlation thoroughly here) should consult the recent matrices (Cheverud, 1982; Shea, 1985b; review by Chernoff and Magwene (1999). As Zelditch, 1987, 1988; Cheverud et al., 1989; a first-order analysis, it is useful to test Wagner, 1989). Such studies have yet to be hypotheses about developmental integra- carried out for models that explicitly focus tion by considering the processes by which on the primate cranial base (but see Chev- different components of a system influence erud, 1995). However, as noted above, a one another. Thus, in the context of cranial high degree of covariation is frequently ev- base growth within the skull, integration ident in interspecific analyses of variation can occur through the direct inductive in the cranial base and other parts of the and/or mechanical effects of neighboring tis- skull. Perhaps the most obvious example of sue-tissue interactions (see Moss, 1997); this phenomenon is the percentage of vari- through secondary effects of growth in one ation in cranial base angle accounted for by region causing changes in the positional re- factors such as brain volume, basicranial lationships among bones in other regions; length, facial angle, and posture. IRE1, and genetically through single genes which which appears to be the dominant factor have effects on multiple regions, or through that influences cranial base angle in pri- the coordinated action of multiple genes via mates, explains 58% of the variation in pleiotropy and linkage (Atchley and Hall, CBA1 and 38% of the variation in CBA4 (see 1991; Cheverud, 1982, 1995, 1996; Zelditch Table 5). Furthermore, according to Ross and Fink, 1995, Zelditch and Fink, 1996; and Ravosa (1993, their Table 2), orbital Chernoff and Magwene, 1999). Of course, axis orientation explains 41% of the varia- the strength of such ontogenetic interac- tion in CBA4 among primates, while facial tions can vary due to changes in the timing orientation explains 22% of the variation in of developmental events, something of great CBA4 among primates. The partial correla- importance for the analysis of heterochrony, tion analysis of Strait and Ross (1999) (dis- as well as due to allometric (size-correlated, cussed above) found that IRE explained 36% size-required) factors. Note that we consider of the variation in CBA1 when the effects of here integration solely in terms of develop- orbital axis and head-neck angle were fac- mental events and processes (e.g., epige- tored out. Further evidence for this sort of netic responses to mechanical loading, dis- complex pattern of covariation is docu- placement due to cell division), but it is mented among humans between CBA, cra- useful to recognize that developmental inte- nial base length, cranial base width, and gration leads to, and is sometimes caused brain volume (Lieberman et al., 2000). by, structural and functional integration. These results are indicative (but not proof) Another problem with assessing any inte- of a pattern whereby multiple factors com- grative role of the cranial base within the bine to influence CBA in such a way that skull is the lack of widely accepted criteria variation in CBA itself may play some role for testing hypotheses of integration. Fol- in modulating the interactions among dif- lowing Olson and Miller (1958) and ferent, spatially separated components of Chernoff and Magwene (1999), we apply the cranium. This hypothesis, however, re- three nonexclusive criteria (correlation, con- quires further testing with comparative on- straint, and ontogenetic sequence) in a pre- togenetic data. 162 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 43, 2000 Constraint. Another expected outcome of gles and spatial relationships occur in the integration is constraint, which is defined skull, and additional research is needed to most generally as a restriction or limitation assess the developmental, structural, and on variation. Regardless of their causes, functional bases of these relationships, and which can be phylogenetic, functional, de- whether they reflect constraints that result velopmental, or structural (Alberch, 1985; from integration. Maynard Smith et al., 1985), constraints are most basically evident in patterns of invari- Ontogenetic sequence. Finally, hypothe- ance. There has not been much work on ses of phenotypic integration may some- phenotypic constraint in the cranial base, times be inferred or tested by examining but several examples suggest it deserves ontogenetic sequences during normal further research. One source of evidence for growth and in the context of controlled ex- constraint is revealed by allometry, which periments. Ontogenetic data allow one to measures size-related conservation of shape test hypotheses of integration by examining (keeping in mind that size-correlated pat- the structural relationships between one terns due to epigenetic and perhaps genetic variable and another during growth (e.g., factors differ from size-required patterns heterochrony, heterotopy), and to compare that have a primarily functional basis). As the pattern and timing of developmental Table 4 (see also Strait, 1999; McCarthy, events. So far, there have been few attempts 2001) illustrates, there are numerous, to examine hypotheses of integration in the strongly correlated ontogenetic scaling rela- cranial base using ontogenetic data (espe- tionships across primates between various cially from embryonic stages), but a few ex- components of the cranial base, the volume amples indicate that the sequence of inter- of neural regions, and facial dimensions. In- actions between the cranial base, the face, tegration between the brain and face via the and the brain are complex and multiphasic, cranial base is implied by the fact that many with the cranial base mediating various in- scaling relationships between contiguous teractions between the face and the brain. anatomical units (e.g., the noncortical brain For example, the prenatal human cranial and the posterior cranial base) result in ad- base initially flexes, then remains stable, ditional strongly correlated scaling relation- and then extends, all during periods of rapid ships between noncontiguous anatomical neural growth (Jeffery, 1999). Postnatally, units, such as those between brain volume the nonhuman primate cranial base (best and facial size. These scaling relationships studied in Pan and Macaca) appears to ex- require more study. tend slightly during the period of neural Another potential source of evidence re- growth, and subsequently extends more garding the presence of a constraint are pat- rapidly and for a long time as the face con- terns of angular invariance. One important tinues to grow. In contrast, the human cra- example is the apparently invariant 90° an- nial base flexes rapidly during the first few gle between the PM plane and the NHA, years of brain growth, and subsequently re- and the limited variability that results from mains stable. These contrasting sequences this relationship on the angle between the imply multiple interactions between the PM plane and both the planum sphenoi- brain and the face via the cranial base, but deum and the anterior cranial base (S-FC) have yet to be resolved in terms of the actual in anthropoids (McCarthy and Lieberman, processes that cause flexion and extension 2001). Other less secure examples of invari- at specific locations during different periods ance may include the relationship between of growth. One hypothesis, which remains cribriform plate orientation and facial ori- to be tested, is that the cranial base func- entation (Ravosa and Shea, 1994), and the tions to accommodate and perhaps coordi- near 45° angle between the external audi- nate these different aspects of growth. Con- tory meatus, the maxillary tuberosities, and trolled experimental studies, which can the midpoint of the orbital aperture (Bro- potentially isolate local and regional effects mage, 1992). Further research, however, is of specific growth stimuli on the cranial base needed on the extent to which invariant an- and the rest of the skull, are a promising D.E. Lieberman et al.] PRIMATE CRANIAL BASE 163 avenue for future research on this problem growth, function, and evolution in primates (see Sarnat, 1982; Bu¨ tow, 1990; Reidenberg and other mammals. and Laitman, 1991). 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