Basicranial flexion relative brain size and facial kyphosis in nonhuman primates.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 91:305-324 (1993) Basicranial Flexion, Relative Brain Size, and Facial Kyphosis in -. Nonhuman Primates CALLUM F. ROSS AND MATTHEW J. RAVOSA Department of Biological Anthropology and Anatomy, Duke Uniuersity Medical Center, Durham, North Carolina 27710 KEY WORDS Encephalization, Klinorhynchy, Anthropoid origins, Hominid evolution Haplorhini, ABSTRACT Numerous hypotheses explaining interspecific differences in the degree of basicranial flexion have been presented. Several authors have argued that an increase in relative brain size results in a spatial packing problem that is resolved by flexing the basicranium. Others attribute differences in the degree of basicranial flexion to different postural behaviors, suggesting that more orthograde animals require a ventrally flexed pre-sella basicranium in order to maintain the eyes in a correct forward-facing orientation. Less specific claims are made for a relationship between the degree of basicranial flexion and facial orientation. In order to evaluate these hypotheses, the degree of basicranial flexion (cranial base angle), palate orientation, and orbital axis orientation were measured from lateral radiographs of 68 primate species and combined with linear and volumetric measures as well as data on the size of the neocortex and telencephalon. Bivariate correlation and partial correlation analyses at several taxonomic levels revealed that, within haplorhines, the cranial base angle decreases with increasing neurocranial volume relative to basicranial length and is positively correlated with angles of facial kyphosis and orbital axis orientation. Strepsirhines show no significant correlations between the cranial base angle and any of the variables examined. It is argued that prior orbital approximation in the ancestral haplorhine integrated the medial orbital walls and pre-sella basicranium into a single structural network such that changes in the orientation of one necessarily affect the other. Gould’s (“Ontogeny and Phylogeny.” Cambridge: Belknap Press, 1977)hypothesis, that the highly flexed basicranium of Homo may be due to a combination of a large brain and a relatively short basicranium, is corroborated. o 1993 Wiley-Liss, Inc. Tarsiers and the extant hominoids, including Homo, differ from most other mammals in having a highly flexed basicranium. A flexed basicranium is one in which the pre- and post-sella portions of the cranial base are downwardly or ventrally deflected relative to each other so that the endocranial and/or exocranial surfaces of those bones do not lie in a single plane, but form a ventrally open angle of less than 180” with each other (Fig. 1). The bony basicranium and the chondrocranium in which it forms are structurally 0 1993 WILEY-LISS, INC. associated with the neurocranium, inner ear, and the roof and walls of the nasal fossa and orbits, as well as articulating with the vertebral column. Consequently, alterations in chondrocranial and basicranical morphology must reflect changes in these functional matrices (Moss, 19721,and it is possible that the basicranium transmits the effects of changes in any one area of the skull to numerous other regions. Received June 14,1991; accepted August 11,1992 306 C.F. ROSS AND M.J. RAVOSA Fig. 1. A comparison of schematic cranial hemisections illustrating correspondence between an increasingly flexed basicranium and increasing size of the brain or brain parts (large clear arrows), change in foramen magnum orientation (small arrows), and orbital axis orientation (large solid arrows). Taxa are, from top to bottom, Tuna, Pun, Austrulopithecus, Homo (modified from Aiello and Dean, 1990.) This possibility has important implications, both for the use of evidence from craniofacial morphology in phylogenetic analyses, and for adaptive and functional interpretations of craniofacial form. Phylogenetic analyses that invoke parsimony to select a pattern of relationships assume that the characters that are used have evolved independently of each other. If characterstate changes in several of these characters can be accounted for with reference to a single underlying mechanism, then scoring them independently may unjustly bias the analysis. More importantly, the possibility that the effects of selection on one part of the skull can be transmitted to other areas in the skull via the basicranium must be considered when developing adaptive explanations for interspecific differences in craniofacial form. Basicranially mediated structural interdependence may confound functional interpretations of correlated changes in different parts of the skull during ontogeny and phylogeny. The separation of functional from purely structural determinants of form is a necessary prerequisite to adaptive interpretations of craniofacial morphology. In light of these considerations, it is hardly surprising that the basicranium has featured prominently in discussions of primate phylogenetic relationships (Dean and Wood, 1981, 1982, 1984; Maier and Nkini, 1984; Shea, 1985, 1988) and craniofacial adaptations (Demes, 1985; Shea, 1985, 1988; Lugoba and Wood, 1990).Adaptive explanations for the evolution of pronounced basicranial flexion in hominids have usually emphasized a correlation between the tendency to extreme basicranial flexion and other “uniquely”human traits, such as bipedal locomotion, pronounced orthognathy, a relatively large brain, and the capacity for encoded speech. The main aim of the research reported here is to evaluate some of these adaptive hypotheses by determining whether tendencies toward highly flexed basicrania in nonhuman primates are correlated with human-like tendencies in posture andlor the relative sizes of the brain and masticatory apparatus. BASICRANIAL FLEXION IN PRIMATES HYPOTHESES 307 Biegert’s hypothesis (1963, p. 122) preAdaptive explanations for differences in dicts that large animals (like Alouatta) will basicranial flexion (bending of the cranial have flat basicrania and small animals (like base so that it is ventrally concave) fall into Saimiri) will have flexed basicrania, merely three groups. Neural hypotheses relate dif- as a consequence of body size a l o n e t h e ferences in basicranial flexion to differences masticatory apparatus scaling with positive in total brain size or in the size of specific allometry and the neocortex with negative parts of the brain. Postural hypotheses ex- allometry against body size. However, he plain differences in basicranial flexion by suggests that this general allometric princihypothesizing how postural differences be- ple “can be circumvented if a specialized extween species necessitate different basicra- pansion of the neopallium (compare Ateles nial morphologies. Facial-orientation hy- and Alouatta) or a specialized reduction of potheses suggest a relationship between the the masticatory apparatus occurs (compare degree of basicranial flexion and the orien- Homo with Pongidae)” (Biegert, 1963, pp. tation of the face. These hypotheses are dis- 122-123). This predicts that size-corrected values for neocortical volume and the size of cussed a t greater length below. the masticatory apparatus should be correlated with size-corrected values for the CBA. Neural hypotheses In addition to these general trends BiegSpatial-packing hypotheses ert argued that a large neocortex relative to Numerous authors have suggested that the size of the masticatory apparatus should phylogenetic increase in relative brain size, be correlated with a n increase in the degree or encephalization, causes a “spatial pack- of basicranial flexion, while a small neocoring“ problem that is solved by flexing the tex relative to masticatory apparatus size basicranium-the cranial base anterior to should be associated with a less flexed basisella being deflected ventrally, or down- cranium. The second version of the spatial-packing ward, and the foramen magnum and postsella cranial base being displaced anteriorly hypothesis is Goulds (1977) suggestion that to accommodate the expanding brain (Fig. 1) increased brain size relative to the length of (e.g., Virchow, 1857; Ranke, 1892; Cameron, the basicranium is the most important 1924, 1925, 1926; Dabelow, 1931; Biegert, cause of increased basicranial flexion and 1957; Delattre and Fenart, 1963; Gould, other “paedomorphic“ features characteris1977). Differences of opinion as to what tic of the human skull (see also Vogel, 1964). brain size should be evaluated against in In support of this hypothesis Gould cited oborder to determine its degree ofencephaliza- servations that human-like features of skull tion underlie two slightly different versions form result when the spheno-occipital synchondrosis, a n important growth site in the of the spatial-packing hypothesis. The first is Biegert’s spatial-packing hy- basicranium, is excised in growing rats (Dupothesis. Biegert (1963) proposed that the Brul and Laskin, 19611, or is pathologically extent of basicranial flexion decreases with missing in a mangabey specimen (Vogel, increasing size of the masticatory apparatus 1964)or chicken embryos (Riesenfeld, 19691. and increases with increasing neocortical Gould’s spatial-packing hypothesis predicts volume. Thus, he predicts a negative correla- that animals with large brains relative to tion between the degree of basicranial flex- the length of the bony basicranium should ion and the size of the neocortex, and a posi- have more flexed basicrania than animals tive correlation between the degree of basic- with relatively small brains. ranial flexion and the size of the masticatory apparatus ( a negative correlation between Cerebellum hypothesis the cranial-base angle [CBA] and another variable being one in which the angle becomes Some workers have suggested th a t a n insmaller and the basicranium more flexed as crease in the size of the cerebellum may act to shift the foramen magnum and post-sella the value of the other variable increases). 308 C.F. ROSS AND M.J. RAVOSA orbits form the floor of the anterior cranial fossa. In such a situation ventral flexion of the orbital axis resulting from the assumption of upright posture must necessarily result in ventral flexion of the floor of the anterior cranial fossa. Dabelow then argued that the resulting basicranial flexion caused an increase in brain size in primates by providing new volume into which the cerebrum could expand. Postural hypothesis The primates offer us several instances in Extreme basicranial flexion in humans which to test Dabelow’s version of the poshas often been attributed to an habitual or- tural hypothesis. Primates are characterthograde posture. The center of mass of the ized by great variation in postural habits as head lies in front of the occipital condyles in well as great variation in the extent of basiprimates, as it does in all mammals cranial flexion and orbital axis orientation (Schultz, 1942). This situation is assumed (Cartmill, 1970, 1972; Ravosa, 1991). Moreby advocates of the postural hypothesis to be over, haplorhines are distinguished from biomechanically inefficient in animals with most strepsirhines in having bony orbits an orthograde posture, an assumption that which are highly convergent and closely apappears to be bolstered by observations that proximated in the midline (Cartmill, 1970, the foramen magnum in extant and fossil 1972). Within the Old World monkey radiahominids is positioned more anteriorly tion, colobines have a relatively broader in(Bolk, 1909; Schultz, 1942, 1955; Ashton terorbital region than cercopithecines (Deland Zuckerman, 1952, 1956; Ashton, 1957; son, 1975). If Dabelow’s postural hypothesis DuBrul, 1977, 1979; Dean and Wood, 1981, is correct then haplorhines and cercopithe1982) and faces more ventrally (Duckworth, cines should exhibit a higher correlation be1915; Bolk, 1910; Moore et al., 1973; Adams tween the degree of basicranial flexion and and Moore, 1975) than in other hominoids. the angle of orbit orientation relative to the The postural hypothesis suggests that in or- post-sella cranial base than seen in strepder to move the condyles closer to the center sirhines and colobines, respectively. The of mass of the entire head, the posterior por- postural hypothesis also predicts that in intion of the cranial base is bent down and terspecific comparisons, animals that habitforward, while the anterior basicranium re- ually adopt more orthograde postures than mains in its original orientation so that the their close relatives will exhibit more highly eyes and face are maintained in a correct flexed basicrania. forward-lookingplane (Fig. 1)(Wood Jones, Facial-orientation hypothesis 1917; Weidenreich, 1924,1941). It has long been speculated that facial poPostural uprightness alone does not appear to require a flexed basicraniurn, how- sition or orientation is in some way structurever. Birds, kangaroos, giraffes, camels, lla- ally associated with the form of the basicramas, and antelopes appear to have little nium (e.g., Virchow, 1857; Ranke, 1892; trouble supporting extremely prognathic Cameron, 1924; Enlow, 1975, p. 203; Siriskulls on erect spines (Schultz, 1942) even anni and Swindler, 1979; p. 88).These specthough many of them have flat or lordotic ulations are indirectly supported by obserrather than ventrally flexed basicrania vations that the rate and timing of growth in (Dabelow, 1929). Dabelow (1929) suggested the anterior cranial base appear to track that ventral deflection of the face concomi- those of the masticatory apparatus (Ashton, tant with postural uprightness should only 1957; Enlow, 1975). The hypothesis regarding the structural be expected to result in basicranial flexion when the bony orbits are highly approxi- association between facial orientation and mated to the midline and the roots of the the degree of basicranial flexion predicts cranial base anteriorly. This presumably results in increased basicranial flexion (Moss, 1958; Aiello and Dean, 1990) as evidenced by the more coronally oriented petrous temporal bones seen in both the “robust” australopithecines and Homo (Dean, 1988). Dean posited that the trend towards an enlarged cerebellum in these hominids may be associated with increased manual dexterity. BASICRANIAL FLEXION IN PRIMATES that the orientations of the lower and upper parts of the face relative to the posterior cranial base should be positively correlated with the orientation of the anterior basicranium relative to the same axis. Primates are ideal for evaluating these hypotheses because various primate taxa, from the level of the suborder to the subfamily, exhibit significant, taxon-specific differences in the orientation of the upper and lower parts of the face, as well as in the degree of flexion of the cranial base. To estimate the reliability of the means we utilized the formula in Box 9.13 of Sokal and Rohlf (1981, p. 263). Using the mean of the standard deviations reported in Table 1 as an estimate of the true standard deviation, at a significance level of 0.05 and infinite degrees of freedom, a sample size of 6 is 80% sure of detecting a difference of 7"-8" between two means. While this sample size does not, therefore, allow fine discrimination between any single pair of means, our analysis is aimed at discerning patterns at taxonomic levels higher than the species. MATERIALS AND METHODS Sample To test these hypotheses, angular and linear measures were taken from lateral radiographs and combined with linear and volumetric measures from the same skulls for which radiographs were available. The radiographs were originally collected by M.J.R. for research on circumorbital morphology in primates but were deemed suitable for the present study because they were taken to ensure that the midsagittal plane of each skull (represented by prosthion, nasion, and basion) was parallel to the film and the collimeter of the x-ray machine. In this way parallactic distortion was minimized. Radiographs of between one and six wildshot adult individuals of 68 species of primates were available, although typically six (three males and three females) were used (see Table 1 for sample sizes). The specimens are housed in the American Museum of Natural History in New York, the National Museum of Natural History in Washington, D.C., the Field Museum of Natural History in Chicago, the Museum of Comparative Zoology in Cambridge, and the British Museum (Natural History), London. The techniques for taking the linear and angular measurements from the radiographs were tested by replicating each measurement five times on radiographs of six individuals of Callicebus moloch. The null hypothesis, that the values for the replicate measurements taken from one individual are the same, was tested and confirmed with analysis of variance (ANOVA) (P < 0.05). 309 Measurements Angular data Angular data (the CBA, angle of facial kyphosis [AFK], and angle of orbital axis orientation [AOA]) were taken from lateral radiographs by tracing the lines defining the angles onto acetate overlaying the radiograph and measuring the angles to the nearest degree with a goniometer and protractor. CBA. Measurements of flexion of the cranial base are usually made from midline structures exposed in hemisected skulls or in lateral radiographs. Because this flexion occurs primarily a t the three basicranial synchondroses (sphenoethmoid, midsphenoidal, spheno-occipital) (see review in Sirianni and Swindler, 19791, flexion was measured in this study using lines that do not cross these synchondroses. Although our CBA therefore differs from the traditional measure of the CBA, we prefer it because it enables interspecific differences in the values for basicranial flexion to be localized to specific synchondroses of the cranial base. Our measurements (Fig. 2) were aimed at capturing the relative orientations of the endocranial surfaces of the clivus ossis occipitalis (CO) and the planum sphenoideum (PSI. Given the difficulties inherent in identifying craniometric landmarks on lateral radiographs, we attempted to approximate those planes that reflect the orientations of these surfaces on dry skuls. The midline endocranial surface of the CO was represented by a line from basion to the posterior edge of the spheno-occipital synchondrosis. When the spheno-occipital synchondrosis was not 310 C F ROSS AND M J RAVOSA TABLE 1 Cranral-base angle, sample s m s , postural categories, and neural sample Taxon Strepsirhini Daubentoniidae Daubentonia madagascariensis Indriidae fndri indri Auahi laniger Propithecus uerreauxi Lemuridae Eulemur fuluus Varecia uariegata Hapalemur griseus Lepilemuridae k p i l e m u r mus6etinus Cheirogaleidae Cheirogaleus major Microcebus murinus Mirza coquereli Phaner furcifer Lorisidae Loris tardigradus Nycticebus coucang Arctocebus calabarensis Perodicticus potto Galagidae Otolemur crassicaudatus Euoticus elegantulus Haplorhini Tarsiidae Tarsius syrichta Platyrrhini Callitrichidae Callithrix argentata Cebuella pygmaea Saguinus fuscicollis Leontopithecus rosalia Callimico goeldis Atelinae Alouatta belzebul Alouatta palliata Ateles fusciceps Ateles geoffroyi Brachyteles arachnoides Lagothrix lagothricha Pitheciinae Pithecia pithecia Chiropotes satanas Cacajao caluus Cebidae Cebinae Cebus apella Cebus capucinus Saimiri sciureus Aotinae Aotus triuirgatus Callicebus moloch Catarrhini Cercopithecoidea Cercopithecinae Cercopithecus aethiops Cercopithecus mona Cercopithecus mitis Miopithecus talapoin Erythrocebus patas Macaca nigra Macaca syluana Theropithecuspelada CBA' mean CBA standard deviation Sample size" Posture3 18 Neural sample4 12 157 7.19 5 P X 168 180 168 5.53 4.59 2.86 6 6 6 0 0 0 X X X 171 177 175 3.01 5.50 3.92 6 6 6 P P 0 X 178 4.08 6 0 X 181 157 158 179 5.94 5.23 P 0 X X - 6 4 1 2 162 171 168 181 0.50 3.31 3.91 4.29 6 6 5 6 P 167 4.23 7.97 6 P 158 6 50 0 147 5.33 6 19 0 164 161 170 173 171 2.42 2.97 2.44 5.68 4.22 6 6 6 6 6 0 186 188 161 162 160 176 5.60 7.09 3.97 7.34 7.29 5.95 6 6 6 6 5 6 P P 182 170 172 4.62 4 09 2.81 6 6 6 0 P P X 173 172 169 5.14 6.15 4.19 6 6 6 P P 0 X X X 180 175 1 26 3.51 P P X 171 170 179 168 167 158 154 151 5.48 3.78 3.06 3.61 6.69 4.63 5 60 4.92 6 6 30 24 13 6 6 6 6 6 6 4 - 6 0 0 P X X ? P 0 0 0 0 P 0 0 0 X X X X X X 10 7 4 P P P X P P X P - P P (continued) 311 BASICRANIAL FLEXION IN PRIMATES TABLE 1. Cranial-base angle, sample sizes, postural categories, and neural sample (Continued) Taxon Lophocebus albigena Cercocebus torquatus Papio anubcs Mandrillus sphinx Mandrillus leucophaeus Colobinae Colobus guereza Piliocolobus badius Procolobus uerus Presbytis cristata Presbytis nielalophos Presbytis rubicunda Presbytas entellus Nasalis laruatus Pygathrrr nemaeus Simzas concolor Rhinopithecus roxeilana Hominoidea Hylobatidae Hylobates muelleri Hylobates lar Symphalangus syndactylus Pongdae Pongo pygmaeus Pan troglodytes Gorilla gorilla CBA' mean CBA standard deviation 163 172 154 144 160 2.13 5.89 5.83 5.32 161 155 157 166 154 152 147 157 144 161 150 4.59 3.93 6.39 2.43 3.76 5.17 5.89 3.78 3.64 4.27 3.97 - Sample size' 6 6 6 6 1 11 6 6 6 6 6 6 6 6 6 6 6 6 Posture3 P P P P P Neural sam~le~ X X 3 P P P P P P P P P X X X P P 3 160 153 167 8.60 6.19 6.83 6 6 6 X 135 152 148 6.46 5.32 1.64 6 6 X 6 X ' Cranial-base angle. 'Sample sizes for angular, volumetric, and linear measures. Linear and volumetric measures were takeu from the same individuals for which radiographs were available. Sample sizes at the species levels represent the number of individuals measured for each species. Sample sizes for taxa above the species level refer to the number of species-means within that taxon. 3Postural categories (0, orthograde; P, pronograde) assigned according to assumptions detailed in text. Categories are relative to other taxa in same Family (Strepsirhini and Hominoidea) or Subfamily (Platyrrhini and Catarrhini) only (Column 1). *Sample sizes for neural measures. Species for which Stephan et al. (1981)give data on neural variables are marked with an 'X".Sample sizes for taxa above the species level represent the number of species within that taxon for which there are data on neural variables. visible in the lateral radiographs, we fitted a line by eye to the endocranial surface of the midsagittal section of the cranial base posterior to dorsum sellae. We believe this method to be reliable, because in those radiographs in which the spheno-occipital synchondrosis was present and visible, the line segment from basion to the posterior edge of dorsum sellae approximated the endocranial surface of the clivus. We recognize the limitations of these radiographically derived measures, and suggest that they may be unsuited for documenting distinctions within species or ontogenetic series, or between closely related species. We do feel however that these measures are useful for documenting broad trends at higher taxonomic levels, as concern us here. The orientation of the pre-sella basicranium was estimated by measuring the orientation of the endocranial surface of the PS (Fig. 2). The posterior point of the PS is de- fined as the apex, or the superiormost midline point on the declivity above the sulcus chiasmatis. Unlike tylion, sella, and the pituitary point, this point lies in the plane of the endocranial surface of the sphenoid. We operationally define the anterior border of the PS as the apex, or superiormost point on the sloping posterior surface of the pit in which the cribriform plate is set. In strepsirhines, this corresponds to the posterior edge of the cribriform plate, or prosphenion. The inferior angle formed by the intersection of the plane of the CO and the plane of the PS is CBA.As this angle decreases the cranial base becomes more flexed and as the angle increases it becomes less flexed. If the angle measures greater than 180" then the PS is retroflexed on the clivus. In order to evaluate Dabelow's postural hypothesis, as well as the facial orientation hypothesis, facial orientation relative to the clivus was quantified using two measures, C.F. ROSS AND M.J. RAVOSA 312 A ans /v- pns B PS ba’ . fn Fig. 2. Diagrams illustrating points used (A) to define planes and angles used (B) in this study as measured from lateral radiographs. CBA,cranial-base angle; AOA,angle of orbital axis orientation; AFK, angle of facial kyphosis; ac, anterior border of CO;ans, anterior nasal spine; ap, anterior border of planum sphenoideum; ba, basion; co, plane of clivus ossis occipitalis; fn, plane of floor of nasal fossa; oa, plane of orbital axis; pns, posterior nasal spine; pp, pituitary point; pps, posterior edge of planum sphenoideum; ps, planum sphenoideum palate and orbit orientation, reflecting the orientation of the lower and upper faces, respectively. AFK. The orientation of the palate relative to the clivus is most consistently represented on lateral radiographs and duplicated across taxa if it is registered as “a line connecting the tips of the anterior and posterior nasal spines (Starck, 1954). Where there is no distinct anterior nasal spine, this line is drawn tangent to the dorsal surface of the midsagittal section of the pre-maxilla” (Cartmill, 1970, p. 63). This plane will there- fore be referred to as the floor of the nasal fossa. The inferior angle formed by the intersection of the plane of the floor of the nasal fossa and the plane of the clivus is referred to as the AF’K, or klinorhynchy (Hofer, 1952). The smaller the AFK, the more kyphotic, ventrally flexed, or klinorhynch the skull. The greater the angle the less kyphotic or more airorhynch (Hofer, 1952) the skull. AOA. The orientation of the orbital axis was determined by the method outlined by Ravosa (1988). The line of the orbital axis BASICRANIAL FLEXION IN PRIMATES was extrapolated anteriorly or posteriorly to the plane of the clivus, and the inferior angle between these two lines is defined as the AOA. Linear measures Linear measures to the nearest tenth of a millimeter were taken from both the radiographs (endocranial basicranial length [BL], prosthion-palate length on the radiographs [PBR]) and the original skulls (prosthionbasion length [PLI, prosthion-basion length on the original skulls [PBSI) using dial and digital calipers. BL. In order to evaluate hypotheses that measures of brain size relative to BL are important determinants of the degree of basicranial flexion, the length of the endocranial surface of the basicranium was measured from the lateral radiographs. Three segments were measured directly from the radiographs: the distances between a) basion and pituitary point; b) pituitary point and the posterior point on the PS (as defined above); and c) the posterior and anterior points of the PS. For each individual, a), b), and c) were then summed and this value converted into an estimate of “actual” BL by multiplying it by PBSPBR. PBR and PBS. Prosthion-basion length on each radiograph (PBR) and on the original skulls (PBS) were measured to calculate the correction factor (PBSPBR) used in calculating BL. PL. The prosthion-staphylion distance was measured to serve as a measure of the size of the masticatory apparatus. Volumetric measures Neurocranial volume. Gould’s spatialpacking hypothesis suggests that overall brain size relative to BL is the prime determinant of the degree of basicranial flexion. Estimates of overall brain size were obtained by measuring the volume of the braincase. The neurocranium was filled with barley through the foramen magnum while shaking it gently from side to side, then it was tapped several times firmly on the side with a finger and filled again. This procedure was repeated until no more barley would fit inside the level of the foramen magnum. The barley in the braincase was then emptied into a graduated cylinder 313 which was shaken until the barley was packed down and formed a level surface at the top. The volume was then read off the graduated cylinder to the nearest ml. Neocortex, telencephalon, and cerebellum volume. The neocortex appears to have increased with positive allometry relative to overall brain size in primate evolution (Passingham, 1975), suggesting that increasing neocortex size relative to BL may be an appropriate measure of relative encephalization. The size of the cerebral hemispheres may also be appropriate-the cerebrum, or telencephalon, includes not only the neocortex, but also its thalamocortical and corticocortical connections, in addition to the archicortex and paleocortex, with their underlying medullary substance or white matter, the basal ganglia, and the lateral ventricle. Thus, the cerebrum represents a morphological level that is intermediate between that of the neocortex and the entire brain. Data on the volume of the neocortex, telencephalon, and cerebellum in 35 of these species were taken from Stephan et al. (1981). Postural behavior Data on postural behavior were taken from the literature (Fleagle, 1977, 1988; Mittermeier, 1978; Fleagle and Mittermeier, 1980; Hunt, 1991). This required two assumptions: first, that animals which leap more also have more orthograde body postures than nonleaping close relatives; and second, that animals with more orthograde body postures also have more orthograde head postures. While acknowledging that these assumptions may be too broad, the relevant data with which to evaluate them are lacking. Broad qualitative distinctions were made between those animals that are often in fairly orthograde postures (sitting, standing, clinging vertically, brachiating) and those that tend to be more pronograde (quadrupedalism, both terrestrial and arboreal). Statistical analyses To test for sexual dimorphism in the CBA, the angle was measured on radiographs of six male and six female Macaca fascicularis and an ANOVA (P < 0.05) used to test for significant differences associated with sex. In Macaca the CBA showed no significant 314 C.F. ROSS AND M.J. RAVOSA added variance component associated with sex. While this does not indicate the absence of sexual dimorphism in the CBA in other taxa, the absence of such dimorphism in a taxon with such extreme body-size dimorphism imples that this may be the case. Consequently, combined-sex species means were used for all analyses. Evaluating Gould’s Spatial-Packing hypothesis involves testing for significant correlations between the size of the CBA and the volume of the neurocranium, neocortex and telencephalon relative to BL. To do this, the ratio of the cube root of each of these neural measures to BL was calculated. The null hypothesis, that there is no skewness in the distributions of these ratios, was tested using formulae in Boxes 7.1 and 7.4 of Sokal and Rohlf (1981: 139 & 174) and confirmed at P < 0.001. The cube root of neurocranial volume/BL constitutes Index of Relative Encephalization 1(IRE1); cube root neocortical volume/BL is IRE2; and cube root telencephalon volume/BL is IRES. To evaluate Biegert’s Spatial-Packing hypothesis that a large neocortex relative to the size of the masticatory apparatus is correlated with a decrease in the CBA, the ratio of the cube root of neocortical volume/palate length (IRE 4) was calculated and tested for skewness (null hypothesis of no skewness was confirmed at P < 0.001). The hypotheses outlined in the introduction were then evaluated by computing Pearson correlations (P < 0.05, see Table 3) for bivariate comparisons between the CBA and the following variables: 1.IREs 1,2, and 3 (Gould’s Spatial-Packing hypothesis); 2. IRE 4 (Biegert’s SpatialPacking hypothesis); 3. cerebellum volume (Cerebellum Hypothesis) (log, and raw CBA); 4. AOA (Postural Hypothesis and Facial-Orientation Hypothesis) (raw variables); and 5. the AFK (Facial-Orientation Hypothesis) (raw variables). These comparisons were performed at the level of the Order (all Primates), Suborder (Haplorhini and Strepsirhini), Infraorder (Platyrrhini and Catarrhini), Superfamily (Hominoidea, Cercopithecoidea) and Subfamily (Cercopithecinae, Colobinae). Partial correlation analyses (P < 0.05) were carried out in order to isolate that proportion of the total variance in the CBA associated with one independent variable while controlling for a correlation with another independent variable. These partial correlation analyses were performed using the natural logs of all variables to enable the angular and cerebellum volume data to be compared with the IREs. Postural data, consisting of categorical or discrete variables, were compared with values for the CBA using a non-parametric Mann-Whitney U-Test (Sokal and Rohlf, 1981). RESULTS Neural theories Bivariate comparisons of IRE1 and the CBA reveal a highly significant negative correlation across primates (r = -0.6451, haplorhines ( - 0.684), platyrrhines (-0.504) and catarrhines (-0.537) (Fig. 3, Table 2). No significant relationship was revealed for strepsirhines. Within catarrhines, significant correlations were observed across colobines (-0.687). Among hominoids, although r = -0.790, the correlation was not significant. These results provide support for Gould’s hypothesis that a large brain relative to basicranial length should be associated with increased basicranial flexion, at least at higher taxonomic levels within haplorhines. Comparisons of IRE2 and IRE3 with values for the CBA reveal significant negative relationships across primates as a whole (IRE2 = -0.540; IRE3 = -0.6061, and haplorhines (IRE2 = -0.567; IRE3 = -0.619). Catarrhines (- 0.640) and cercopithecoids (-0.769) also show significant negative correlations between IRE3 and the CBA. Strepsirhines do not show a significant relation. It is interesting to note that, although these relationships were not significant, IREs 2 and 3 were negatively related to the cranial base angle in hominoids and cercopithecines (with high “r”s),but positively related in colobines. The negative correlations indicate that as neocortex and cerebrum size relative to basicranial length increase across all primates, the CBA decreases. This provides only weak corroboration for hypotheses that the sizes of the neocortex and cerebrum relative to basicranial length are associated with increased basicranial flexion. The BASICRANIAL FLEXION IN PRIMATES 315 Tarsius CALL I T R l C H l D A E ATELINAE PlTHECllNAE CEBIDAE CERCOPITHECINAE COLOBINAE HYLOBAT I DAE PONGIDAE IRE1 Fig. 3. Plot of the angle of basicranial flexion vs. IRE 1 (ratio of cube root of neurocranial volume to basicranial length) in haplorhine primates. TABLE 2. Correlation coefficients for biuariate cornparisom evaluating hypotheses Cranial-base angle (CBA) vs CBA raw (R) or log, (L) Primates Strepsirhini Haplorhini Platyrrhini Catarrhini Hominoidea Cercopithecoidea Cercopithecinae Colobinae IRE1 IRES IRE3 IRE4 R & (L) R R R Cerebellum volume rawhog, W(L) -0.606*** -0.32911s -0.619** 0.23111s -0.640* -0.49011s -0.769* -0.909ns 0.419ns 0.0720ns -0.205ns 0.35511s -0.624* -0.038ns 0.920ns -0.13311s 0.83411s -0.769ns -0.466**/-0.300ns -0.318nd0.022ns -0.464*/-0.286ns 0.011ns/0.314ns -0.455nd-0.517ns -0.940nd-0.84911s -0.343nd-0.36411s -0.917nd-0.968* 0.720nd0.735ns -0.540** -0.32911s -0.567** -0.lOlns -0.504* -0.537** -0.59711s -0.50911s -0.79011s -0.335ns(L) -0.70711s 0.203ns(L) -0.92911s 0.603ns -0.687* -0.645*** -0.36011s -0.684*** AOA AFK R R 0.608*** 0.469*** 0.379ns 0.42211s 0.617*** 0.429*** 0.723*** 0.465* 0.34611s -0.03311s 0.443ns 0.054ns 0.746*** 0.232ns 0.853*** 0.746*** 0.784** 0.36011s IREl, ratio ofcube root of neurocranial volume to BL; IRE2 ratio of cube root of neocortical volume to BL; IRE3 ratio of cube root of telencephalon volume to BL, IRE4 ratio of cube root of neocortical volume to P L AOA, angle of orbital axis orientation; AFK, angle of facial kyphosis. All analyses were performed using raw values, except where noted with (L) h e . , Cerebellum volume vs CBA and two comparisons of CBA and IRE1). * P i 0.05;**P< 0.01; ***P < 0.001; ns = P > 0.05. break-down of these relationships within hominoids may be attributable to low sample sizes. The lack of a significant correlation between IRE2 and CBA across cercopithecoids is due to the presence of opposing trends within the constituent subfamilies. Biegert’s Spatial-Packing hypothesis predicts that the CBA should be positively correlated with increasing palate length (i.e., the angle should get larger and the basicranium less flexed). Bivariate comparisons reveal that across all primates, haplorhines, catarrhines, and cercopithecines the CBA actually decreases, and the basicranium becomes more flexed, as palate length increases (Fig. 4, Table 3). Bivariate comparisons provide some support for Biegert’s suggestion that increasing neocortical volume should be associated with a decreasing CBA, the predicted relationship being seen across primates and haplorhines as a whole, but only when raw data are used (Table 3). Biegert’s Spatial-Packing hypothesis also predicts that increasing neocortex size relative to the size of the masticatory apparatus will be negatively correlated with the CBA. Across primates the correlation between neocortical volume and palate length is significant and negatively allometric (r = 0.889; slope = 2.45). Bivariate comparisons reveal the ratio of neocortical volume to palate length (IRE 4) and the CBA to be significantly negatively related only among platyrrhines (-0.624). These results provide C.F. ROSS AND M.J. RAVOSA 316 . . . . . . . . . . . . 525s c + lsl X 5 2- 0 w J z W 4 w 9m s ‘ 0 s O x 0 PONGIDAE A O . 0 0 m+ A & & A A U a 0 0 0 ’A Q -rn .V -0 0 0 I- 2z 5 0 5 . V W %“Q 1 IS. I 0 lsl 0 Tarsius CAILITRICHIDAE ATELINAE PlTHECllNAE CEBIDAE CERCOPITHECINAE COLOBINAE HYIOBATIDAE W 08 0 (R v A 5. - A ”1 4 9 . . 22s 2 5 . . . . . . . . . . .V. 275 3 32s 35 37s 4 42s 4s t 47s log PALATE LENGTH Fig. 4. Plot of the angle of basicranial flexion vs. palate length (loge)in haplorhine primates. Relation ship across strepsirhines is not significant. See Table 2 and text. only very limited support for Biegert’s hypothesis that a large masticatory apparatus relative to neocortical volume is associated with increased basicranial flexion. Aiello and Dean (1990) suggest that increasing cerebellum size may serve to deflect the posterior portion of the cranial base anteriorly, resulting in greater basicranial flexion. Comparisons between log-transformed values for the CBA and cerebellum size reveal no significant relationship for any taxonomic group save cercopithecines (-0.968) (Table 2). Using raw values, cerebellum volume is negatively correlated with the CBA across primates (-0.466) and haplorhines (-0.464), providing some support for the Cerebellum Hypothesis. Among homninoids, the correlation coefficients for this bivariate comparison are high but not significant, suggesting that increased sample size might confirm this hypothesis in this group. Postural Hypothesis Dabelow’s hypothesis, that increased flexion is associated with ventral deflection of the face when the orbits are highly approximated in the midline, is corroborated. As predicted, there is a significant positive relationship between the CBA (the orientation of the pre-sella relative to the post-sella cra- nial base) and the orientation of the orbits relative to the post-sella cranial base among haplorhines (0.6171, but not among strepsirhines (Table 2; Figure 5). Platyrrhines also show a positive correlation between basicranial flexion and orbit orientation (0.723). This relationship is not found among catarrhines overall, but it is found in cercopithecoids (0.7461, cercopithecines (0.853) and colobines (0.784). Moreover, as predicted, cercopithecines show a higher r-value than is seen in colobines, indicating that there is a closer correlation between the angle of flexion and orbit orientation in the former than the latter. Demonstration of a relationship between basicranial flexion and orbit orientation corroborates Dabelow’s hypothesis, but it does not necessarily support the prediction of the postural hypothesis that basicranial flexion should be associated with orthograde head and body postures. MannWhitney U-Tests within families and subfamilies revealed that atelins (i.e., Ateles, Brachyteles, Lagothrix) are the only taxa which utilize orthograde body postures (suspension) and exhibit more flexed basicrania than closely related forms with more pronograde habits (i.e., Alouatta). This result does not provide strong support for the postural hypothesis. not significant,P > 0.05 -0.473**/0.300ns -0.326ns/-O.O12ns -0.471*/-0.257ns - 0.005ns/- 0.301ns -0.424nsi-0.404ns -0.802ns/-0.747ns -0.154ns/-O.O91ns -0.890ns/-0.938ns 0.726ns/0.734ns -0,514**"/-0,387*** -0.026ns/-O.l93ns -0.507***/-0.389** -0.167ns/-O.O94ns -0.503**/-0.543*** -0.694nd-0.68311s -0.335nd-0.375* -0.722***/-0.726*** -0.576*/-0.589* -0.334**/-0.254* 0.234nd-0.30411s -0.321*/-0.236ns 0.330nd0.354ns -0.416*/-0.410* -0.613ns/-0.600ns -0.186ns/- 0.190ns -0.615*/-0.602* 0.155nd0.142ns -0.415***/-0.363** 0.227nd0.273ns -0.423***/-0.384"* 0.293nd0.304ns -0.320*/-0.295ns -0.625ns/-0.588ns -0.156ns/-O.l34ns -0.706***/-0.716*** 0.011ns/O.O06ns = Neocortical volume rawflog, (XI Neurocranial volume rawflog, (XI Basicranial length rawflog, (XI Palate length raw/log, (XI * P < 0 05; **P < 0.01: ***P < 0,001; ns Primates Strepsirhini Haplorhini Platyrrhini Catarrhini Hominoidea Cercopithecoidea Cercopithecinae Colobinae Cranial-base angle vs. TABLE 3. Correlation coefficients for bivariate comparisons between the cranial-base angle and linear and neural variables -0.506"*/-0.381* -0.327ns/-O.O06ns -0.494*/-0.342ns 0.772*/0.828* -0.428nd-0.415ns -0.809nd-0.75311s -0.169nd-0.114ns - 0.890nd- 0.939ns 0.700ndO.705ns Telencephalon volume raw/log, (XI C.F. ROSS AND M.J. RAVOSA 318 . . . . . . . . . . w. 1 9 0 - ' - ' 1 X. . 0 O w 0 X X T w Q 1 6 Tarstus N CALLlTRlCHlDAE W ATELINAE X PlTHECllNAE 0 CEBIDAE 0 CERCOPITHECINAE A COLOBINAE W HYLOBATIDAE V PONGIDAE V 1304.. 145 150 . . . . . . . . . . . . 155 160 165 170 175 180 185 ORBITAL AXIS ORIENTATION (DEGREES) 190 195 Fig. 5. Plot of raw values of the angle of basicranial flexion vs. the angle of orbital axis orientation in haplorhine primates. Relationship across strepsirhines is not significant. See Table 3 and text. 190, . . . . c + X 180. ,-. 0 0 170. W n - X 0 0 A O m v) W % , _1 W $160. Q A 0 0 0 m 150. I 110 X A T i md eg A#. 0 0 0 0 ATv A 3 130 0 140 I50 160 ANGLE OF FACIAL KYPHOSIS (DEGREES) 120 O ATELINAE PlTHECllNAE CEBIDAE CERCOPITHECINAE COLOBINAE HYLOBATIDAE PONGIDAE A,* 0 wo L Q 4Po Tarslus CALL I TR IC H ID A € 170 0 180 Fig, 6. Plot of raw values of the angle of basicranial flexion vs. the angle of facial kyphosis in haplorhine primates. Relationship across strepsirhines is not significant. See Table 3 and text. Facial-orientation hypothesis Partial correlation models The orientation of the palate is significantly positively correlated with the CBA at the ordinal level (0.469) (Table 2, Fig. 6). At the subordinal level only haplorhines show a significant relationship (0.422) and, within haplorhines, platyrrhines (0.465)and cercopithecines (0.746)show this relationship but catarrhines as a whole do not. All independent variables found to be significantly correlated with the CBA in bivariate comparisons were included in partial correlation models evaluated at all taxonomic levels within haplorhines (where necessary). Because none of the variables considered here were significantly correlated with the CBA across strepsirhines and BASICRANIAL FLEXION IN PRIMATES among hominoids, partial correlation models were not tested within these taxa. Similarly, across catarrhines only IRE 1is significantly related to the CBA, so partial correlation analyses were not performed. (Partial correlation models incorporating interaction terms were not significant at any taxonomic level, so multiple regressions were not required.) Partial correlations between the CBA and both palate orientation and orbit orientation at all taxonomic levels within haplorhines revealed that, independent of orbital axis orientation, palate orientation accounts for none of the variation in the CBA. These results provide no support for the assertion that palate orientation is an important determinant of the CBA. Across primates (0.7321, haplorhines (0.816), and among colobines (0.940) the most parsimonious partial correlation model (i.e., the one with the highest correlation coefficient and significant independent variables) includes the angle of orbital axis orientation (positively correlated) and IRE 1 (negatively correlated). Across platyrrhines neuriocranial volume relative to basicranial length explains none of the variance in the cranial base angle when the angle of the orbital axis is taken into account. For catarrhines and cercopithecoids, the best model included only telencephalon volume relative to basicranial length (IRE 3), which is negatively correlated with the CBA. Across cercopithecines only the AOA is included in the most parsimonious model explaining variance in the CBA. DISCUSSION Neural hypotheses Gould (1977) suggested that brain size relative to BL is a more important cause of the degree of basicranial flexion than brain size relative to other (unspecified) measures. As predicted by this hypothesis, at several taxonomic levels within haplorhines an increase in overall brain size relative to the length of the basicranium is associated with an increase in basicranial flexion, although it remains to be determined whether this association reflects a causal connection between these variables. Regardless, flexion 319 effectively increases neurocranial volume without increasing BL, in a fashion analogous to increasing the proportion of a sphere which is utilized without increasing the sphere’s diameter. Gould’s spatial-packing hypothesis is supported by observations that juvenile primates tend to have larger brains relative to body and skull size than their adult stages (Gould, 19751, as well as having more flexed basicrania. Nonhuman primate cranial ontogeny is characterized by a decrease in both relative brain size and the degree of flexion, whereas in human ontogeny the relatively large brain and flexed basicranium seen in the juvenile are retained into adulthood (Ashton and Zuckerman, 1952, 1956; Zuckerman, 1955; Schultz, 1955; Ford, 1956; Moore et al., 1973;Adams and Moore, 1975). As an explanation for extreme basicranial flexion in humans, Gould’s spatial-packing hypothesis is supported by observations that the human cranial base is “anteroposteriorly compressed relative to that of other extant hominoids due to “both a reduction in the length of the sphenoid bone” and “the forward displacement of the foramen magnum and occipital condyles” (Dean and Wood, 1984, p. 70). Cross-sectional data on basicranial growth in extant hominoids suggest that these “shorter lengths of the human cranial base . . . result from a reduction in the early postnatal spurt and an early cessation of growth that continues in the apes after growth has ceased in Homo sapiens” (Dean and Wood, 1984, p. 176). The comparative data presented here provide some corroboration for Gould’s spatial-packing hypothesis, but data on human basicranial flexion are required to confirm it, This study found little evidence to suggest that variation in neocortex or volume relative to BL accounts for variation in the CBA in haplorhines. There is more evidence t o suggest that telencephalon volume relative to BL is an important determinant of the CBA in catarrhines. That there was not greater concordance between the results for the different IRES is surprising, considering that relative neurocranial volume is correlated with the degree of flexion, and that anthropoids have more neocortex and telencepahlon relative to brain size than prosimi- 320 C.F. ROSS AND M.J. RAVOSA ans (Passingham, 1975, 1982). This may be facial orientation explains the extreme dedue to the fact that anthropoids exhibit “a gree of basicranial flexion in humans, then larger increase in gyrification for every unit why do lagomorphs and orangutans apparincrease in body or brain weight or neopal- ently reorient their face without modifying lial volume” than prosimians (Zilles et al., the cranial base? Dabelow argued that a shift to an or1989, p. 143). Whereas brain weight and volume are the best predictors of neocortical thograde posture should only result in ingyrification among prosimians, neocortical creased basicranial flexion, in association volume is more important among anthro- with ventral deflection of the face, in those poids. Thus, increases in neocortical volume animals with highly approximated bony orin anthropoids may be accompanied by in- bits. Dabelow’s hypothesis predicts a close creases in gyrification, rather than in- correspondence between orbital axis oriencreased neurocranial volume and increased tation and the CBA in haplorhines but not in strepsirhines, haplorhines in general havflexion of the cranial base. There is only limited evidence at present ing narrower interorbital regions relative to to support the contention of Aiello and Dean skull length than strepsirhines. This predic(1990) and Moss (1958) that increased cere- tion is supported. In strepsirhines with bellum size is a major cause of increased highly approximated bony orbits, like Loris basicranial flexion. Biegert’s (1963) sugges- tardigradus, the narrowest interorbital distion that the degree of flexion is determined tance lies above the olfactory tract, not beby the size of the neocortex relative to the low it, as in haplorhines (Cartmill, 1972).In masticatory apparatus is also not corrobo- strepsirhines, therefore, the orientation of the anterior limb of the basicranium need not rated. covary with orbital axis orientation as the Postural hypothesis medial orbital walls are not closely applied The hypothesis that postural uprightness to the basicranium. Similarly, because they alone necessitates a flexed basicranium is have a narrower interorbital distance, cercorefuted by cases where reorientation of the pithecines show a closer correlation between face appears to have occurred without re- orbital axis orientation and the CBA than quiring correlated changes in the orienta- colobines, as well as showing a correlation tion of the anterior part of the cranial base. between CBA and AFK not seen in colobines. Although orbit orientation is correlated Ventral flexion of the face relative to the braincase in posturally upright lagomorphs with the degree of basicranial flexion in hapis not associated with flexion of the cranial lorhines, it remains to be determined base (DuBrul, 1950; Plate 2). Within Old whether differences in either of these craWorld monkeys, colobines have more dor- nial angular values are determined by possally deflected (airorhynch) faces than cer- tural differences. The postural hypothesis copithecines, although they have similar de- asserts that phylogenetic changes in body grees of basicranial flexion (Ravosa and orientation require alterations in visual axis Shea, 1993). Similarly, the orangutan, orientation in order to maintain the eyes in Pongo, has an extremely airorhynch face the forward-facing plane. These alterations (i.e., dorsally deflected) relative to the Afri- are presumably achieved by changing the can hominoids Pan and Gorilla, but it has orientation of both the bony orbits and the much greater flexion of the cranial base. pre-sella basicranium relative to the postThat the face has rotated up and backwards sella cranial base, thus resulting in changes relative to the basicranium in Pongo is in- in the degree of basicranial flexion, either as dicated by several features of the anterior an essential part of the reorientation of the cranial fossa, such as stenosis or pinching of bony orbits (Wood Jones, 1917) or as a pleiothe nasofrontal ethmoidal area (Montagu, tropic effect (Dabelow, 1929). This hypothesis explains the condition in 19431, reduction of the sphenoidal sinuses (Cave and Haines, 1940) and the cribriform posturally upright lagomorphs and kangaplate, and an increased frequency of meseth- roos, which have their orbits well separated moid-presphenoid articulation (Montagu, in the midline, but it does not explain the 1943) (reviewed in Shea, 1985, p. 336). If situation in Pongo. Pongo has a narrow in- BASICRANIAL FLEXION IN PRIMATES terorbital region when compared to the African apes and Homo, in combination with an airorhynch face and a highly flexed basicranium. Nor does it make sense of the situation in birds. Dabelow’s postural hypothesis only makes sense if the orbital approximation in birds and Pongo occurred after reorientation of the face in phylogeny, or if it follows the establishment of spatial relationships between the neurocranium and splanchnocranium during ontogeny. The most serious objection to the postural hypothesis is that most mammals, and certainly primates, have flexible necks which enable them to reorient their visual axes in the frontal plane by flexing and extending the whole head. Assuming that this option is indeed available to all primates, is natural selection likely to alter circumorbital morphology, resulting in profound reorganization of the neurocranialhplanchnocranial boundary and the olfactory, respiratory, and masticatory systems? The answer to this question must await the gathering of data on head posture and visual axis orientation relative to the neck and trunk in living primates. Meanwhile, although we have supported Dabelow’s prediction that orbital orientation and basicranial flexion should be correlated in animals with highly approximated bony orbits, the only taxon in which we found a significant relationship between posture and the degree of flexion was atelines. Atelines also exhibit a significant negative relationship between IRE1 and the CBA (r = -0.887; p = .045) however, suggesting that relative brain size may be determining flexion in these animals. In any event, the postural hypothesis does not provide a general explanation for basicranial flexion among primates. Facial orientation These comments notwithstanding, the observed correlation between orbit orientation and basicranial flexion in animals with highly approximated orbits does imply that facial orientation may be affected by basicranial morphology. Although palate and orbit orientation are significantly correlated with each other across all primates (Ravosa, 1991) and both are significantly correlated with the CBA across Haplorhini, the partial correlation analyses indicate that palate ori- 321 entation explains none of the variation in the CBA when orbital axis orientation is taken into account. Partial independence in the orientation of upper and lower facial skeletons is also indicated by Ravosa’s (1988, 1991) work on browridge morphology in primates. Ravosa found that among cercopithecoidsthe orientation of the orbital axis relative to the basicranium is significantly correlated with anteroposterior dimensions of the supraorbital torus. This indicates that anteroventral rotation of the orbital margins results in increased disjunction between neural and orbital cavities, necessitating the development of a supraorbital torus to roof the orbits. Ventral deflection of the palate, however, is not correlated with anteroposterior browridge dimensions in any primates, even though it is correlated with orbital axis orientation. Ravosa’s results, and those reported here, suggest that the significant correlations observed in bivariate comparisons between palate orientation and the CBA are merely due to palate orientation tracking orbital axis orientation. In addition to showing covariance of orbital axis orientation and the CBA, extant anthropoids also share the rare combination of highly frontated and convergent bony orbits (Cartmill, 1970). In most animals the degree of orbital convergence, or the extent to which the two orbital axes are parallel, varies inversely with orbital frontation (or the degree of verticality of the orbits). This is not the case in haplorhines. Tarsiers and anthropoids not only have relatively parallel orbital axes, but they also have more vertically oriented orbital rims than strepsirhines. This morphological combination brings the medial walls of the orbital cones into close approximation, forming, in small haplorhines, an apical interorbital septum situated immediately ventral to the cribriform plate and the anterior limb of the basicranium. It is probably as a direct result of this structural integration of the medial orbital wall and the pre-sella basicranium that the orientations of the orbital axes and the anterior limb of the basicranium are found to covary in interspecific comparisons among haplorhines. It remains to be determined why haplorhines combine greater orbital conver- 322 C.F. ROSS AND M.J. RAVOSA gence with greater orbital frontation. Cartmill (1970) noted that a positive correlation between the degree of orbital frontation and convergence is also seen in indriids. Indriids share with haplorhines the possession of relatively broad frontal lobes (Radinsky, 1968), and Cartmill suggested that at least some of the frontation seen in anthropoids may be due to an anterior expansion of the neocortex pushing the superior orbital margin forward, expansion which could also cause ventral deflection of the orbital axes. However, as Cartmill himself pointed out, this does not explain the situation in large anthropoids, like cercopithecoids and hominoids, which, due to the negative allometry of brain on body size, have relatively small brains for their body size, yet maintain highly frontated orbits in spite of the fact that the resulting disjunction between neural and orbital cavities must be bridged with bone (Ravosa, 1988, 1991). If increased brain size relative to BL influences basicranial flexion, and in turn, ventral deflection of the orbital axes, why does the brain not expand out over the orbits, utilizing the space that its own expansion creates? This may be due to increase in the size of parts of the brain that do not lie over the orbits, such as the occipital, parietal, and temporal lobes, or the cerebellum. Partial correlation analyses across haplorhines and colobines certainly indicate that increasing overall brain size (as measured by total neurocranial volume) has an effect on the CBA independent of orbital axis orientation. CONCLUSIONS Although this study of the correlates of basicranial flexion perhaps raises as many questions as it answers, it does provide new insights into the changes in craniofacial morphology occurring at the origins of anthropoids and humans. The last common ancestor of all anthropoids, and maybe the last common ancestor of anthropoids and extant tarsiers, appears to have had a combination of features that can be claimed to constitute a new Bauplan. Most important for subsequent changes in anthropoid craniofacial morphology was the approximation of the bony orbits in the midline, creating strutural interdependence between the anterior cranial base and fossa, and the underlying orbital cavities. Large brain size relative to BL, possibly due to an increase in the size of the neocortex of the temporal and occipital lobes, was associated with increased flexion of the cranial base and associated ventral deflection of the orbital axes and upper face. Determination of whether these traits are synapomorphies of a clade containing only anthropoids and tarsiers, synapomorphies of a broader haplorhine clade sensu (Szalay et al., 19871, or convergences (Simons and Rasmussen, 1989, Rasmussen, 1990) must await the discovery of more fossils. Certainly, these modifications in the spatial relationships between the orbits and the neurocranium provided room for expansion of the frontal lobes in later evolutionary lineages. Gould’s spatial-packing hypothesis as an explanation for the extreme basicranial flexion seen in humans is supported by the comparative evidence presented here. Corroboration with the comparative method is the most powerful means of rendering putative human “uniquenesses”nonunique, and therefore intelligible. Human uniquenesses are not explicable, exactly because they are unique (Cartmill, 1990). However, many morphological features believed to be unique to humans, basicranial flexion for example, are explicable because they are not unique in themselves, but represent extreme instantations of rules and principles that underlie the generation of form across primate taxa. Because demonstration of that nonuniqueness involves comparisons with other animals, such morphological features can only be explained by using the comparative method. The comparative data provide little support for the idea that orthograde head and body postures require a flexed basicranium, although confirmation of this must await more detailed information on postural behavior in living primates. We suggest that the high degree of basicranial flexion in humans can be explained as an extreme instance of a general rule that large brains relative to BL tend to be associated with increased basicranial flexion. ACKNOWLEDGMENTS C.F.R. thanks Dr. John Carmen, Department of Anatomy, Auckland Medical School, BASICRANIAL FLEXION IN PRIMATES Auckland, New Zealand, for his enthusiastic support at the inception of this project. The authors also thank Drs. Matt Cartmill and Bernard Wood, as well as two anonymous reviewers, for helpful comments on a n earlier draft of this paper. The authors greatly appreciate the timely comments of Dr. Bill Jungers. This research was supported by grants to C.F.R. from the National Science Foundation (BNS-9100523) and the Duke University Graduate School, and grants to M.J.R. from the National Science Foundation (BNS-8813220), the National Institutes of Health (DE055951, Northwestern University (0100-510-110Y),and the American Museum of Natural History. 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