Int J Primatol DOI 10.1007/s10764-015-9886-5
Implications of the Relationship Between Basicranial Flexion and Facial Orientation for the Evolution of Hominid Craniofacial Structures Dimitri Neaux 1 & Emmanuel Gilissen 2,3,4 & Walter Coudyzer 5 & Franck Guy 1
Received: 27 January 2015 / Accepted: 9 November 2015 # Springer Science+Business Media New York 2015
Abstract The basicranium and face have been linked through genetic, developmental, and functional relationships throughout their evolution. As a result, basicranial morphology most likely plays a major role in the evolution of facial structures. We describe the relationships between basicranial flexion and the face in Homo, Pan, and Gorilla to determine the role of cranial base angle reduction in the setup of the short and orthognathic face of Homo. We test the hypotheses that cranial base flexion plays a significant part in variation in facial orientation, length, and projection at the intraspecific level. The sample comprised 125 crania of adult specimens including 66 Homo sapiens, 32 Pan troglodytes, and 27 Gorilla gorilla. We described the cranial base and face using landmarks placed on scans of the surfaces and computed correlations between the cranial base angle and facial orientation, length, and projection. Our results support the hypotheses that cranial base flexion plays a significant part in facial orientation for Homo and Pan and in facial length for Pan. The hypothesis that basicranial flexion is related to a reduction of facial projection is not supported. The findings suggest that basicranial flexion can explain several anatomical specificities of hominins, including the reduction of prognathism and the reduction of the length of the
* Dimitri Neaux
[email protected] 1
Institut de Paléoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironnements UMR CNRS 7262, Université de Poitiers, 86073 Poitiers, France
2
Department of African Zoology, Royal Museum for Central Africa, B-3080 Tervuren, Belgium
3
Université Libre de Bruxelles, Laboratory of Histology and Neuropathology, B-1070 Brussels, Belgium
4
Department of Anthropology, University of Arkansas, Fayetteville, AR 72701, USA
5
Department of Radiology, University Hospitals Leuven, B-3000 Leuven, Belgium
D. Neaux et al.
nasopharynx. We found different patterns in the different genera, highlighting the fact that changes in the relationship between craniofacial structures may have occurred during hominid evolution. Keywords Cranial base . Cranium . Facial block . Facial projection . Hominin
Introduction Extant Homo possesses unique craniofacial features when compared to Pan and Gorilla, their closest extant relatives. The face is short and orthognathic in Homo and is associated with a short and flexed cranial base. Basicranial flexion is defined as the flexion in the sagittal plane of the ethmoid, the sphenoid, and the basilar part of the occipital bone (Lieberman and McCarthy 1999; Spoor 1997). It characterizes the relative position of the anterior, middle, and posterior cranial fossa (Lieberman and McCarthy 1999). The configuration in Homo contrasts greatly with those of Pan and Gorilla, which have large protruding faces associated with long and slightly flexed cranial bases. Several of the characters observed in Homo are already present in early members of the human lineage. Descriptions of Sahelanthropus tchadensis (Brunet et al. 2002; Guy et al. 2005; Zollikofer et al. 2005) from Chad, dated at 7 Ma (Lebatard et al. 2008), and Ardipithecus ramidus from Ethiopia, dated at 4.4 Ma (Kimbel et al. 2014; Suwa et al. 2009; White et al. 2009), suggest that these extinct taxa exhibit trends inherent to the human family: a reduction of the face associated with a shortening and a flexion of the cranial base. The evolutionary processes allowing the establishment of hominin craniofacial trends remain largely unknown. To characterize the mechanisms permitting the establishment of a short face, we need to take into account the fact that the structures composing the cranium are not independent of one another. Cranial structures interact in many ways —genetic, developmental, functional, and evolutionary— that lead to the morphological integration of craniofacial features (Cheverud 1982; Klingenberg 2010; Olson and Miller 1958; Wagner 1996). Because of these interactions, variation in some localized structures, such as the cranial base, can cause morphological changes in other craniofacial traits, such as the face, and vice versa. The face and cranial base are adjacent structures as the roof of the orbits is also the floor of the anterior cranial fossa, i.e., the depression in the floor of the cranial vault which houses the frontal lobes (Enlow and Azuma 1975). Based on this spatial proximity and taking morphological integration into account, researchers have hypothesized that basicranial flexion is likely to play a major role in the evolution and the development of facial structures at the interspecific level (Basili et al. 2009; Biegert 1963; Enlow and Azuma 1975; Kuroe et al. 2004; Lieberman 2000; Ross and Henneberg 1995; Simpson 2005; Weidenreich 1941). These hypotheses link basicranial flexion to facial characteristics such as facial orientation, facial length, and facial projection. The facial orientation hypothesis states that the face is characterized by a structural unit called the Bfacial block,^ composed of the frontal bones, the anterior cranial fossa, and the ethmomaxillary complex, i.e. the ethmoid bone, the maxillary bone, and the hard palate (McCarthy and Lieberman 2001). This hypothesis takes into account the
Relationship Between Basicranium and Face
fact that the orientation axis of the orbits defined by the neutral horizontal axis (NHA; Fig. 1, Table I) is always very similar to the orientation of the anterior cranial base, which is also the superior limit of the face. It further predicts that the angle between the posterior limit of the facial block, defined by the posterior maxillary plane (PM; Fig. 1), and NHA is always close to 90° (Bromage 1992; Enlow and Azuma 1975; Enlow and Hans 1996; McCarthy and Lieberman 2001). Therefore, if the PM–NHA angle is constant (Fig. 1), a downward rotation of the anterior cranial fossa may lead to a downward rotation of the entire facial block (McCarthy and Lieberman 2001). In this case, basicranial flexion should cause a Bmechanical^ downward and backward rotation of the face. The facial length hypothesis predicts a significant relationship between cranial base flexion and facial length (FL; Lieberman et al. 2008; McCarthy 2001). FL is defined by the length of the anterior facial plane (AFP; Fig. 1, Table I) segment. As the face grows downward and forward relative to the cranial base, a shorter face will be related to a more flexed cranial base to maintain the cohesion of craniofacial structures. The facial projection hypothesis relates flexion of the cranial base to a reduction in facial projection (FP; Fig. 1, Table I) (Lieberman 2000). FP, the anteroposterior position of the orbits and of the outer table of the frontal bone relative to the cranial base, is a major aspect of craniofacial shape as it influences the position of the face relative to the basicranium. Flexion of the cranial base should rotate most of the facial structures under the anterior cranial base (Lieberman et al. 2000; Weidenreich 1941) and thus may limit FP. The aim of this work is to assess the relationships between cranial base flexion and facial orientation, FL, and FP by testing these three hypotheses. We examined Homo and its two closest relatives (Pan and Gorilla) to establish a comparative framework. We test the hypotheses within each genus to determine whether the relationships previously described at the interspecific level (Lieberman 2000; McCarthy 2001; McCarthy and Lieberman 2001) also exist at the intraspecific level.
Fig. 1 Sagittal cut of the cranium of a modern human showing the measurements used in the present study. CBA = cranial base angle; PM = posterior maxillary plane; NHA = neutral horizontal axis; FP = facial projection; AFP = anterior facial plane; 1 = foramen caecum; 2 = sella turcica; 3 = basion; 4 = PM point; 5 = pterygomaxillare; 6 = orbital margin; 7 = orbital axis; 8 = nasion; 9 = prosthion.
D. Neaux et al. Table I Definition of cranial measurements used in the present study Measurement
Abbreviation
Definition
Cranial base angle
CBA
Measured between the foramen caecum, the sella turcica, and the basion
Posterior maxillary plane
PM plane
Measured between the PM point and the pterygomaxillare
Neutral horizontal axis
NHA
Measured between the orbital margin and the orbital axis
Anterior facial plane
AFP
Measured between the nasion and the prosthion
Facial projection
FP
Measured between the nasion and the foramen caecum
Materials and Methods Materials We summarize the information concerning the sample in Table II. All specimens are dentally mature, with third molars in full occlusion. The following institutions house the cranial material: the Royal Museum for Central Africa (Tervuren), the Anthropological Institute and Museum (University of Zurich), and the Natural History Museum (London). Data Acquisition We scanned each cranium using a medical computerized tomography (CT) scanner, with voxel sizes and slice thicknesses adjusted according to the cranial size of each specimen. Voxel sizes range 0.3–0.7 mm and slice thicknesses range 0.3–1 mm. F. Guy, E. Gilissen, and W. Coudyzer acquired the CT images of the specimens. We computed the CT scan data using Avizo v6.0 software (©Visualization Sciences Group). We extracted bone material from the virtual volume using automatic thresholding. As the specimens are dry, this step is relatively straightforward. The digitized skulls present mainly empty spaces and material information corresponding to the bone. We converted the corrected volumes into three-dimensional polygonal surfaces for analysis.
Methods Definitions We provide the definitions of the measurements and of the landmarks used in the study respectively in Tables I and III. The reduction of the cranial base angle
Table II Description of the sample used in the present study: Number of females, number of males, and total number for Homo sapiens, Pan troglodytes, and Gorilla gorilla Taxa
Female
Male
Total
Homo sapiens
34
32
66
Pan troglodytes
17
15
32
Gorilla gorilla
13
14
27
Relationship Between Basicranium and Face Table III Count, name, and definition of the cranial anatomical landmarks used in the present study Count Landmark
Definition
1
Foramen caecum Most anterior and inferior midline point of the anterior cranial base
2
Sella turcica
3
Basion
Most anterior and inferior midline point on the margin of the foramen magnum
4
PM point
Midsagittal projection of the most anterior point of the superior orbital fissure
5
Pterygomaxillare Midsagittal projection of the most posterior point of the alveolar process on the inferior surface of the maxilla
6
Orbital margin
Midsagittal projection of the landmark passing by the middle of the segment constituted by the inferior and superior borders of the orbits
7
Orbital axis
Midsagittal projection of the point, which is the center of the segment between the superior orbital fissure and the inferior border of the optical canal
8
Nasion
Midline intersection of nasal and frontal bones
9
Prosthion
Most anterior midline point of the maxillary alveolar process
Midpoint between the sphenoidale (most superior and posterior midline point on the tuberculum sellae) and the dorsum sellae (most superior and posterior midline point on the dorsum sellae)
(CBA) is commonly used to describe basicranial flexion (Fig. 1, Table I; Cousin et al. 1981; Lieberman and McCarthy 1999; McCarthy 2001; Spoor 1997). When defined between the foramen caecum, the sella turcica, and the basion, it is sometimes called CBA 1 (Lieberman and McCarthy 1999). The foramen caecum, which is used to define CBA 1, is part of the anterior cranial fossa, which is in direct anatomical contact with the face via the orbital part of the frontal and the small wings of the sphenoid (Enlow and Azuma 1975). Thus, because of the proximity between the foramen caecum and the facial structures, CBA 1 is suitable for the study of the relationships between basicranium and face. We characterize the face using four measurements: 1) PM–NHA characterizing the orientation of the posterior face, 2) PM–AFP defining the orientation of the anterior face, 3) the length of the AFP segment characterizing FL, and 4) FP (Fig. 1). Acquisition We described the cranial base and face using 3D landmarks placed on the surfaces using Landmark v3.0 software (Wiley et al. 2005). To test for intraobserver landmark repeatability, we sampled five specimens of each taxon twice and evaluated the measurement errors by MANOVA. We found no significant differences between the repeated samples for Homo (Wilks’ λ = 0.03, F = 4.20, df = 8, 1, P = 0.36), Pan (Wilks’ λ = 0.00, F = 24.69, df = 8, 1, P = 0.15), and Gorilla (Wilks’ λ = 0.03, F = 3.99, df = 8, 1, P = 0.37), indicating that for each taxon the measurement error was smaller than the variation within the sample. We computed the measurements of the CBA, PM–NHA, and PM–AFP angles and of the FL and FP lengths from the 3D landmark coordinates using R (R Development Core Team 2015) with a code specifically written for these analyses. Statistics First, we computed ANOVAs to test for differences between taxa for each measurement. We calculated an initial ANOVA including the three studied taxa. Where the difference across all genera was significant, we performed ANOVAs between pairs
D. Neaux et al.
of genera as post hoc tests to define clearly where the effect of genus lies. We can expect static allometry (Gould 1966) between males and females in extant great apes (O’Higgins and Dryden 1993; Rosas and Bastir 2002). We performed an ANOVA between the sexes for each measurement to assess the influence of sexual dimorphism. We computed correlations between CBA on the one hand and PM–NHA, PM–AFP, FL, and FP on the other hand using a Pearson’s correlation coefficient. We calculated correlations within each genus to test the relationships at the intraspecific level.
Results Differences Between Taxa Mean CBA, PM–AFP, FL, and FP values are significantly different across the three taxa, and between each pair of genera (Table IV). Values for the PM–NHA angle are not statistically different across the three taxa. Sexual Dimorphism There are significant differences in CBA and FL between the sexes in all three taxa (Table V). There is a significant difference between sexes in Homo and Gorilla in FP values and in Pan and Gorilla for the PM–NHA angle. There are no significant differences between the sexes for PM–AFP values. Correlations Between Basicranial Flexion and Facial Measurements Homo displays a significant negative correlation between CBA and FP (Table VI). For Pan, there is a significant positive correlation between CBA and FL. Finally, Gorilla displays a significant negative correlation between CBA and PM–AFP. All other correlations were nonsignificant.
Discussion Our results support the facial orientation hypothesis in Homo and Pan. The PM–NHA angle is not significantly different between Homo, Pan, and Gorilla and is not significantly related to the CBA in these three taxa. The PM–AFP angle is not significantly related to the CBA in Homo and Pan. Our findings support the facial length hypothesis in Pan where the reduction of the cranial base angle is significantly related to a shortening of FL. Finally, the facial projection hypothesis is not supported at the intraspecific level, as no taxon displays a significant positive correlation between CBA and FP. Considering the results of the facial orientation hypothesis, when the cranial base flexes the orientation of the face relative to the PM plane remains constant. These results are in line with a previous study (McCarthy and Lieberman 2001) that found that the face forms a structural unit, the facial block, composed of the frontal bones, the
Relationship Between Basicranium and Face
Table IV Results of ANOVAs comparing the values of CBA, PM-NHA, PM-AFP, FL, and FP between all taxa (Homo, Pan, and Gorilla)
Degrees of freedom
F
P-value
All
2, 123
251.8
