Locomotion and Basicranial Anatomy in Primates and Marsupials
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Locomotion and Basicranial Anatomy in Primates and Marsupials
Catalina I. Villamil Dickinson College
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Recommended Citation Villamil, Catalina I., "Locomotion and Basicranial Anatomy in Primates and Marsupials" (2017). Dickinson College Faculty Publications. Paper 830. https://scholar.dickinson.edu/faculty_publications/830
This article is brought to you for free and open access by Dickinson Scholar. It has been accepted for inclusion by an authorized administrator. For more information, please contact [email protected]. Locomotion and basicranial anatomy in primates and marsupials
Catalina I. Villamil
Department of Anthropology, Dickinson College, PO Box 1773, Carlisle, PA, 17013
Center for the Study of Human Origins, Department of Anthropology, New York University, 25
Waverly Place, New York, NY 10003, USA
New York Consortium in Evolutionary Primatology, New York, New York, 10024, USA
Corresponding author:
E-mail address: [email protected] (C.I. Villamil)
Keywords: Basicranium, Locomotion, Orthogrady, Posture, Hominin, Convergent evolution
Funding sources:
This work was supported by a Wenner-Gren Foundation Dissertation Fieldwork grant [Gr.
9110], a New York University Antonina S. Ranieri International Scholars Fund travel grant, and a New York University Global Research Initiative Fellowship.
1 Abstract
There is ongoing debate in paleoanthropology about whether and how the anatomy of the cranium, and especially the cranial base, is evolving in response to locomotor and postural changes. However, the majority of studies focus on two-dimensional data, which fails to capture the complexity of cranial anatomy. This study tests whether three-dimensional cranial base anatomy is linked to locomotion or to other factors in primates (n = 473) and marsupials (n =
231). Results indicate that although there is a small effect of locomotion on cranial base anatomy in primates, this is not the case in marsupials. Instead, facial anatomy likely drives variation in cranial base anatomy in both primates and marsupials, with additional roles for body size and brain size. Although some changes to foramen magnum position and orientation are phylogenetically useful among the hominoids, they do not necessarily reflect locomotion or positional behavior. The interplay between locomotion, posture, and facial anatomy in primates requires further investigation.
Abbreviations:
PCA = Principal components analysis
CVA = Canonical variates analysis
2BPLS = Two-block partial least squares
BSB = Basion-sphenobasion length
BOS = Basion-orbitosphenoid length
BCA = Basion to midpoint of bicarotid line
BBT = Basion to midpoint of bitympanic line
SBB = Sphenobasion breadth
2 NAP = Nasion-prosthion (face) length
PPP = Prosthion-posterior palate length
PBR = Palate breadth
SBO = Sphenobasion-basion-opisthion angle
NBO = Nasion-basion-opisthion angle
PBO = Posterior palate-basion-opisthion angle
3 Introduction
The basicranium is an important region of the skull, serving as a site of interaction between the many varied functions of the head and those of the postcranium. In hominins, the basicranium underwent a fairly drastic reorganization in its orientation and relationship to the face, with alterations to the morphology of the temporal and occipital bones (Kimbel et al.,
2014). Among those features said to differ in hominins and hominoids is the position of the foramen magnum, which is often argued to indicate locomotor or positional behaviors.
Specifically, the foramen magnum is argued to be more anterior (e.g., Şenyürek, 1938; Schultz,
1955; Dean and Wood, 1981; Schaefer, 1999; Russo and Kirk, 2013, 2017) and more inferiorly oriented (e.g., Moore et al., 1973) in bipeds than in quadrupeds. As a result, basicranial morphology, and foramen magnum position specifically, is often used to assess locomotor and positional behaviors, especially in fossil remains when postcranial elements are missing.
Important examples include Sahelanthropus (Brunet et al., 2002, Zollikofer et al. 2005) and
Ardipithecus ramidus (White et al., 1994), and notably in Dart’s (1925) initial assessment of the
Taung skull, the holotype of Australopithecus africanus.
An anterior position of the foramen magnum has long been linked to differences in head balance and neck musculature (reviewed in Schultz, 1942; Dean, 1985; Luboga and Wood, 1990) and is argued to confer a mechanical advantage to orthograde taxa (Şenyürek, 1938; Schultz,
1942, 1955). More anteriorly placed foramina magna may reduce the amount of nuchal musculature required to sustain the head in an upright posture by shifting the center of gravity of the skull (Şenyürek, 1938). Differences between humans and other hominoids in the size and position of muscles with origins on the basicranium have been attributed to shifts in foramen magnum position (Dean, 1985). The rectus capitis anterior muscle in humans, for example, is
4 further from the midline and not anterior to the foramen magnum, while the longus capitis is shorter and oriented transversely, rather than anteroposteriorly as in other hominoids (Dean,
1985). Both these muscles are tied to flexing and supporting the head. The more inferior orientation of the foramen magnum found in hominins relative to the posterior orientation in other hominoids has also been attributed to the more vertical orientation of the cervical vertebral column in bipeds (Moore et al., 1973). Variation in the orientation of the foramen magnum has been tentatively tied to cervical lordosis in humans (Been et al., 2014), providing a direct link between cranial base morphology and posture. This relationship between the cranial base and posture remains even though cervical lordosis itself is primarily a result of soft tissue structures
(Been et al., 2014).
However, the true relationship of foramen magnum position and orientation to posture and locomotion across taxa remains contested (Bolk, 1909; Moore et al., 1973; Lieberman et al.,
2000; Kimbel and Rak, 2010; Russo and Kirk, 2013, 2017; Ruth et al., 2016). Strait and Ross
(1999) found no clear evidence that head and neck postures are influencing basicranial morphology in primates. Further, many primates, including monkeys and apes, appear to have undergone a shift in foramen magnum anatomy relative to other mammals so that the foramen magnum is oriented more inferiorly rather than posteriorly, regardless of whether they remain primarily quadrupedal (Le Gros Clark, 1934). Such a shift, with a more centralized and inferiorly oriented foramen magnum, may have been present in the ancestor of all modern anthropoids (Le
Gros Clark, 1934). Instead of reflecting aspects of locomotor behavior, foramen magnum position and orientation may instead be related to aspects of brain size, brain growth and brain restructuring (Le Gros Clark, 1934; Weidenreich, 1941; Biegert, 1963; Lieberman et al. 2000), cranial vault shape (Bolk, 1909), or anatomy and positioning of the face (Le Gros Clark, 1934;
5 Ruth et al., 2016). Luboga and Wood (1990) also found an allometric influence on basicranial morphology—in humans, individuals with larger crania have more posteriorly located foramina magna.
Le Gros Clark (1934) argued that an increase in the size of the occipital lobes of the brain, linked to improved vision in primates, resulted in a posterior growth of the cranial vault and thus the repositioning of the foramen magnum on the basal aspect of the skull. This repositioning of the axis of the head in turn is linked to the repositioning of the face (Le Gros
Clark, 1934). Ross and Ravosa (1993) and Lieberman et al. (2000) confirmed a link between brain size and cranial base angulation in primates, although these data do not generally match ontogenetic data, which shows that cerebral expansion does not account for changes to basicranial morphology (reviewed in Bastir et al., 2010).
Biegert (1963) argued based on ontogenetic data that a combination of a relatively larger face and smaller brain would result in a less flexed cranial base. Bastir et al. (2010) found support for this hypothesis in primates and in fossil hominins, in particular those showing that larger faces and smaller brains are both linked to a more posteriorly rotated cranial base. Mice with relatively larger faces also tend to have longer cranial bases, and the size of the face accounts for a substantial portion of variation in cranial base angulation (Lieberman et al., 2008).
More recent studies (e.g., Neaux, 2017) have also found links between the length, size, and orientation of the face and basicranial features.
This latter set of hypotheses, in which foramen magnum orientation is linked to brain size and facial anatomy, is supported by a variety of indirect data as well. For example, primate juveniles display more anterior, inferiorly oriented foramina magna than their adult counterparts despite no real differences in cervical orientation (Bolk, 1909; Moore et al., 1973), suggesting
6 that there is no locomotor or positional component to foramen magnum orientation. Additionally, adult Pongo have a more vertical cervical column than other hominoids, but the position and orientation of their foramen magnum is indistinguishable from that of knuckle-walking hominoids (Moore et al., 1973), and the orientation of the foramen magnum among anthropoids is not associated with orientation of the orbit or measures of head and neck carriage (Strait and
Ross, 1999; Lieberman et al., 2000). Adult Alouatta, however, display exceptionally posteriorly positioned and oriented foramina magna, which Bolk (1909) hypothesized are linked to their well-developed hyoid apparatus. Orthopedic data in humans also suggests a link between masticatory anatomy and cervical posture (e.g., Özbek and Köklü, 1993; Tecco and Festa, 2007), further suggesting at least some interplay between the different regions of the skull and the orientation of the foramen magnum within taxa.
It is unclear how these relationships of brain size and facial size to basicranial anatomy are linked to the morphologies associated with locomotion and posture. Recent research into craniofacial growth, development, and modularity provide strong evidence that the skull is a highly integrated structure in which changes to one feature will affect many others (e.g., Bastir and Rosas, 2005, 2009; Lieberman et al., 2008; Martínez-Abadías et al., 2009; Bastir et al.,
2010). Integration likely extends into the head and neck (Ross and Ravosa, 1993), suggesting a complex relationship between posture and skull shape.
I use three-dimensional data of the cranial base and face to investigate the relationship of foramen magnum position and orientation to locomotor behavior in primates and marsupials in order to consider morphological change in the foramen magnum in the context of the cranium as a whole. I test two primary hypotheses: 1) the foramen magnum is more anteriorly positioned in orthograde or bipedal taxa than in pronograde taxa and 2) the foramen magnum is more
7 inferiorly oriented in orthograde or bipedal taxa than in pronograde taxa. Marsupials serve as a comparative group in which to test and verify hypotheses about foramen magnum anatomy that have been constructed primarily for primates because, like primates, marsupial taxa engage in a variety of postures and locomotor behaviors, including orthogrady and bipedalism. Bipedal rodents are excluded due to the unique morphology of their basicrania, which include greatly expanded auditory bullae (e.g., Ruth et al. 2016), and the difficulty of collecting microscribe data on such small animals.
I additionally test other factors potentially related to foramen magnum orientation
(Weidenreich, 1941; Biegert, 1963; Luboga and Wood, 1990; Lieberman et al., 2000). These factors include overall body size, facial size and orientation, and brain size. Specifically, I test whether they are linked to the morphology of the cranial base and whether facial size is linked to locomotion and posture.
Materials and methods
The sample consists of 223 individuals from 11 strepsirhine genera, 250 individuals from nine catarrhine genera (Table 1), and 231 individuals from eight marsupial genera (Table 2). All individuals are adult and maturity was assessed through both dental eruption and fusion of the sphenooccipital synchondrosis and other sutures, as necessary. Samples consist of approximately equal numbers of males and females generally. Species were chosen to represent different locomotor or postural behaviors and balance phylogenetic relationships. Phylogenetic trees for primates were downloaded from 10kTrees Version 3.0 (Arnold et al., 2010; see Supplementary
Online Material [SOM] Figs. 1 and 2). The phylogenetic tree for macropods is based on the trees presented in Cardillo et al. (2004) and Meredith et al. (2008, 2009; SOM Fig. 3), and does not
8 include branch lengths. The human sample consists of approximately equal numbers of native
Ugandans and Zulu. Among primates, an attempt was made to use only one species for each genus or to keep different species separate in analyses, but in the case of Eulemur, Nycticebus, and Propithecus this proved impossible because a substantial portion of museum specimens were classified as species that have recently been split and renamed using soft tissue or geographical characteristics that were not available in museum records or collections. As a result, multiple species are grouped together for each genus, although an attempt was made to include only members of the Eulemur fulvus and Propithecus verreauxi groups and to exclude definite
Nycticebus javanicus and Nycticebus pygmaeus.
Locomotor and positional designations are based on a review of the available literature and are based on the primary locomotor or positional behaviors of each taxon (Tables 1 and 2).
Although locomotor designations are an imperfect estimate of positional behavior or head posture in life, and taxa with different positional behaviors generally maintain similar neck postures (e.g., Vidal et al., 1986; Graf et al. 1995), it is difficult to assess head posture directly without a living reference animal. The locomotor and positional designations used here should by no means be considered absolute but should instead be considered as generalized trends.
Taxa are considered orthograde when they are habitually or obligately upright, regardless of locomotor mode. These include vertical clingers and leapers (galagos, Hapalemur, indriids), brachiators (hylobatids), and bipedal humans, as well as koalas, which spend most of their time in upright sitting postures (Grand and Barboza, 2001). Taxa are considered pronograde when they habitually or obligately hold their spines in horizontal, rather than vertical, positions.
Although Gorilla and Pan display a variety of adaptations to orthograde postures, when necessary they are analyzed with pronograde quadrupeds, as in previous literature (e.g., Russo
9 and Kirk, 2013). The great apes are not separately analyzed as a group with orthograde Homo and hylobatids because this results in a purely phylogenetic grouping. However, in some cases I have analyzed them as a third “mixed” group. Similarly, bipedal marsupials are not strictly orthograde and often maintain pronograde postures despite locomoting on two limbs. When necessary, bipedal marsupials and orthograde koalas are analyzed both together as an
‘orthograde’ group and separately as ‘bipedal’ and ‘orthograde’ taxa, respectively.
Orthograde and bipedal taxa are considered separately, as Russo and Kirk (2013) found that the position of the foramen magnum is more anterior in both orthograde, non-bipedal taxa and bipedal, non-orthograde taxa (kangaroos and wallabies), compared to closely related pronograde quadrupeds. Orthogrady has been argued to result in shifts of basicranial anatomy due to a repositioning of the cranium relative to the body axis (Şenyürek, 1938; Schultz, 1942,
1955; Moore et al., 1973; Luboga and Wood, 1990). However, if bipedal macropods, which are not orthograde, display similar basicranial morphologies as orthograde taxa, it could mean that bipedalism influences foramen magnum orientation independently of orthogrady. Macropods provide an excellent taxon in which to test these differences because they include an orthograde, quadrupedal taxon (koalas) as well as pronograde bipeds. These bipedal macropods engage in high frequencies of quadrupedal or pentapedal (tail-assisted) postures, as well as bipedal locomotion (Windsor and Dagg, 1971). Bipedalism, in particular, is rare among mammals, which makes macropods an important comparative group for testing hypotheses about bipedalism from an evolutionary (rather than experimental) perspective. However, it is important to note that marsupials differ from other mammals in patterns of both dental eruption and ossification of the cranial bones (reviewed in Ruth et al., 2016), and in this way, they may not represent a good comparative group for primate cranial morphology.
10 The majority of these locomotor designations are straightforward, however, other authors may contest some of the designations chosen here. Designations that differ from previous studies are as follows: Otolemur crassicaudatus, considered as pronograde by Russo and Kirk (2013), is considered here to display mixed locomotion and posture due to its occasional use of vertical leaps and “kangaroo-like” locomotion along with high frequencies of quadrupedal movement, which differentiates it from both Euoticus and Galago, which are considered to be vertical leapers, and lorisids, which are considered to be slow arboreal quadrupeds (Bearder and Doyle,
1974; Crompton, 1984). Eulemur is considered to display mixed locomotor behaviors following
Gebo (1987), as Eulemur of all species typically spend about a third of their locomotor bouts moving quadrupedally and another third leaping, unlike both Varecia variegata and Lemur catta, which favor quadrupedal locomotion and forelimb assisted climbing.
Landmark data were collected directly on the cranium of each individual using a
Microscribe G digitizer. Landmarks encompass the morphology of the face, basicranium, and vault, and include regions that are thought to vary between taxa with different locomotor behaviors. A full list of the 43 landmarks is available in the SOM (SOM Table 1, SOM Fig. 4).
Additional linear and angular data were measured with calipers or extracted from the original coordinate data (Table 3). I standardized linear measurements of the cranial base by the nasion- opisthocranion length in order to compare relative lengths while avoiding the influence of palate size. Including the length of the palate in an estimate of cranial length, when the purpose is to standardize basicranial measures, artificially inflates differences between taxa that have substantially different facial morphologies but may not otherwise differ in their basicranial morphologies. These linear measurements are standardized by nasion-opisthocranion and not the geometric mean because the aim is to estimate the proportion of cranial length that is anterior
11 and posterior to the foramen magnum, and not to estimate relative size. This is especially important since the face is hypothesized to influence basicranial anatomy. I standardized sphenobasion breadth (SBB) by the basion-sphenobasion length (BSB) to determine relative breadth, and standardized palate breadth (PBR) by the prosthion-posterior palate length (PPP). In order to test whether position and orientation of the foramen magnum are linked to brain size, species means for brain volume and body mass data were taken from the literature (Stephan et al., 1981; Kappelman, 1996; Leonard et al., 2003; MacLean et al., 2009; Isler, 2011; SOM
Tables 2 and 3). Species designations are unknown for the Papio sample used here, so the averages of Papio anubis and Papio ursinus were used. Brain volume and body mass data are unavailable for Chlorocebus pygerythrus, so the means for Cercopithecus mitis, an available taxon of similar body size that is phylogenetically close to Chlorocebus, were used here. Brain volume was standardized using a simple ratio of brain volume to body mass rather than an encephalization quotient, because the aim was to assess the size of the brain as a proportion of overall body size as per Biegert’s (1963) original hypothesis, rather than to assess relative differences in encephalization between taxa.
Landmark data were analyzed using 3D geometric morphometrics methods in MorphoJ
(Klingenberg, 2011). Raw coordinate data are submitted to a Procrustes analysis, in which differences in size or orientation (when digitized) between individuals are removed. Because many of the landmarks collected here are bilateral, shape variation can be partitioned into symmetry (between-individual) and asymmetry (within-individual) components. Because the purpose of this study is not to study asymmetry explicitly, only the symmetric component of shape variation was used for subsequent analyses. This symmetric shape variation was submitted to principal components analysis (PCA), which reduces variation to a series of orthogonal
12 vectors that can be visualized graphically. PCA results were then used to perform a canonical variates analysis (CVA), which takes into account known group membership and can provide statistical measures of differences between groups. CVA were performed using ‘orthograde’
(including orthograde, suspensory, vertical clinging/leaping, and bipedal taxa), ‘pronograde’
(including antipronograde and quadrupedal taxa), and ‘mixed’ (when appropriate) as the known groups (see Tables 1 and 2) and used all available PC scores. I also performed MANOVA to estimate Pillai’s statistic and test differences between groups using the same locomotor categories as in CVA, again using all available PC scores. Geometric morphometric analyses were performed twice: once with basicranial landmarks only and once with both basicranial and facial landmarks. Obvious outliers and individuals with incomplete data were removed in all cases.
To ascertain the role of phylogeny in morphology, I used a comparative method in which
I compared closely related taxa with different locomotor behaviors—for example, I compared the sister taxa galagids to lorisids and the sister taxa indriids to lemurids, and then ascertained whether patterns persisted across clades. I did not use phylogenetic PCA, because the scores derived from phylogenetic PCA are not independent of phylogeny and still reflect phylogenetic differences (Polly et al., 2013). Further, removing the phylogenetic component of shape will remove the aspects of shape that are adaptive, when adaptation corresponds to phylogeny (Polly et al., 2013). This is potentially the case for some of the taxa used in this study. For example, indriids form a clade separate from lemurids, but indriids as a whole differ from lemurids in their positional behavior. Similarly, hylobatids form a clade separate from the hominids, but the hylobatids as a whole differ from the hominids in their positional behavior. Instead, regular PCA results were mapped onto a phylogeny to test whether there is a significant phylogenetic
13 component to the results, and significance was determined by performing 10,000 randomized permutations. Mapping PCA results onto a phylogeny also serves to illustrate possible convergence among taxa.
When necessary for interpretation, marsupial wireframes were oriented using actual skulls and articulated skeletons that approximate realistic postures, with the nasion-prosthion segment aligned with photographs of living animals. The Frankfurt horizontal is inappropriate for these taxa, and marsupials do not have bony orbital rings or closures that can be used as a reference for orientation. For primates, wireframes are presented using landmarks on the external auditory meatus for orientation. I do not use the Frankfurt horizontal because Strait and Ross
(1999) found, in a study of living primates, that the Frankfurt horizontal is not applicable to non- human primates. Instead, the orbital plane better approximates head orientation in primates
(Strait and Ross, 1999). The landmarks on the primate external auditory meatus were collected to reflect the superior-inferior orientation of the orbital plane, although the relationship is imperfect.
Regardless, the geometric morphometrics results presented in PCA and CVA are independent of orientation.
In addition, I performed two-block partial least squares (2BPLS; Klingenberg, 2009) to test whether the cranial base and face covary within marsupials, strepsirhines, and catarrhines.
2BPLS provides an RV coefficient that is a multivariate analog of R2 and represents an estimate of overall covariation between blocks (Klingenberg, 2009). Within each of the groups analyzed
(marsupials, strepsirrhines, and catarrhines), the data were pooled by genus. Pooling this way allows covariance estimates to be made relative to genus means, rather than on absolute values, providing what is essentially an estimate of average covariation within the sample. The 2BPLS was performed on two blocks—the cranial base and the face—from within a single landmark
14 configuration. This means that the two blocks are not independent since they have been subjected to the same Generalized Procrustes Analysis, but MorphoJ performs additional statistical procedures to take the non-independence of these landmarks into account before estimating covariance (Klingenberg, 2009). I used landmarks from within a single configuration because the relationship of the landmarks in the face to those in the basicranium, particularly in terms of orientation, is in itself important. Significance for the 2BPLS analyses was determined by performing 250 randomized permutations.
PC1 and PC2 for each analysis, which account for over half the morphological variation in the sample, were correlated to relative brain size and to logged centroid size to determine the presence and strength of allometric effects on shape. These analyses were performed on both unpooled data and on pooled data (Klingenberg, 2016). For the pooled analyses, data were pooled by genus using MANOVA, and the PC and centroid size residuals from this analysis were then used to perform a correlation analysis. Correlations were performed in general at the suborder level and at the superfamily level for primates. Homo was excluded from analyses at the superfamily level because initial results suggest it is highly unusual and does not reflect general primate trends. Other non-coordinate data were analyzed using standard statistical methods on R 3.1.1 (R Core Team, 2016) and JMP® 12.1.0 (SAS Institute, Inc.). For two-group comparisons, I used Welch’s t-test. For three- or four-group comparisons, I used Tukey’s HSD test.
Results
Primates
15 In strepsirhines, PC1 and PC2 together account for 57.2% of variation (Fig. 1, SOM
Table 4). Taxa with larger positive values along PC1 (galagids and lorisids) tend to have relatively shorter (basion to orbitosphenoid) and wider (auriculare to auriculare) basicrania. The region around the foramen magnum is convex in these taxa, the external auditory meatus extends inferiorly past the plane of the basioccipital, and the jugular foramen is almost parallel to the midline (Fig. 1C). Taxa with larger negative values along PC1 (lemurids and indriids) tend to have relatively elongated basicrania (basion to orbitosphenoid) and the region around the foramen magnum is more concave (Fig. 1C). The external auditory meatus does not extend past the basioccipital, and the jugular foramen is perpendicular relative to the midline (Fig. 1C).
Along PC2, taxa with larger positive values (Varecia, Lemur, and the lorisids) tend to have more posteriorly oriented and more convex foramina magna, as well as external auditory meatuses that are relatively more anterior to the foramen magnum (Fig. 1C). Taxa with zero or negative values
(Eulemur, Hapalemur, indriids, and galagids) tend to have more inferiorly oriented, concave foramina magna and external auditory meatuses that are closer to, but not necessarily overlapping with, the foramen magnum (Fig. 1C). There is no clear separation among taxa along
PC3 and PC4, so these are not discussed here.
Among strepsirhines, taxa that engage in more orthograde behaviors (Euoticus, Galago,
Hapalemur, Avahi, Indri, Propithecus) tend to display more inferiorly oriented foramina magna, but also more inferiorly oriented occipital squama (see PC2, Fig. 1). This trend is most evident when comparing species means, in which Hapalemur griseus, an orthograde lemurid, converges with the indriids (Fig. 1B). Taxa that engage in intermediate frequencies of orthograde behaviors
(Otolemur, Eulemur) tend to display intermediate morphological positions that overlap with both orthograde and pronograde groups. Orthograde and pronograde taxa are statistically
16 distinguishable from each other, as are taxa with mixed behaviors, which are intermediate between orthograde and pronograde taxa in a CVA plot (p < 0.0001; see SOM Fig. 5), as well as using MANOVA (Pillai = 1.5593, F = 18.013, d.f. = 336, p < 0.001). However, there is substantial morphological overlap among taxa (Fig. 1A).
In catarrhines, PC1 and PC2 together account for 55.1% of variation (Fig. 2, SOM Table
4). Taxa with more positive scores along PC1 (hylobatids) tend to have relatively longer anterior basicrania (basion to orbitosphenoid) and shorter squamous occipitals (opisthion to opisthocranion), as well as more posteriorly oriented foramina magna, while those with more negative scores (all other catarrhines, but particularly Homo and Papio) tend to have shorter anterior basicrania and longer squamous occipitals, as well as more inferiorly oriented foramina magna (Fig. 2C). Along PC2, taxa with more positive values (cercopithecoids) tend to have more vertically oriented occipital squama than those with more negative values, as well as external auditory meatuses that overlap with the foramen magnum anteroposteriorly. Hylobatids and
Homo both have more negative scores along PC2, which represents more horizontally oriented occipital squama and external auditory meatuses that are more anteriorly positioned relative to the foramen magnum (Fig. 2C). PC3 does not separate taxa either taxonomically or by positional behavior, and PC4 does not distinguish any taxa from each other and so are not discussed further.
Like orthograde strepsirhines, humans and hylobatids both display somewhat more inferiorly oriented foramina magna than other catarrhines, as well as more inferiorly oriented occipital squama (see PC2, Fig. 2). However, along PC2, hylobatids also overlap substantially with Chlorocebus, which are primarily pronograde, and Pan paniscus (Fig. 2A). Humans are, however, unique from all other taxa in that they have an occipital nuchal plane that is relatively larger and extend posteriorly to a greater degree than in other taxa, as well as extremely
17 inferiorly oriented foramina magna (Fig. 2). Humans and the larger bodied catarrhines also tend to display an anterior shift in the position of the foramen magnum, so that basion is less distant from or anterior to the external auditory meatus than in smaller taxa including gibbons (Fig. 2C).
Orthograde and quadrupedal taxa are statistically distinguishable from each other in both CVA
(p < 0.0001; see SOM Fig. 6) and MANOVA (Pillai = 0.91175, F = 56.533, d.f. = 197, p <
0.001), and when Gorilla and Pan are considered as a separate category that is neither orthograde nor quadrupedal (Pillai = 1.802, F = 49.797, d.f. = 394, p < 0.001).
In addition to similarities in the orientation of the foramen magnum, orthograde strepsirrhines and catarrhines both display a ‘bend’ at sphenobasion, which can be defined as the basion-sphenobasion-orbitosphenoid angle (Figs. 1C and 2C). This likely reflects differences in the position of the face relative to the occipital and likely reflects the degree of basicranial flexion in these taxa.
There are significant differences in angular and linear measurements between orthograde/bipedal and pronograde/quadrupedal taxa among primates (Table 5; SOM Tables 5–
6). However, there is substantial overlap among different taxa and no discernible patterns linked to locomotor or positional behaviors when the data are compared more closely (Figs. 3–4). It is possible that among catarrhines, where hylobatids are the only non-human, non-quadrupedal taxon, there is a phylogenetic trend driving some of these apparent differences. In SBO and PBO, humans fall close to other large-bodied hominoids but hylobatids have substantially lower angles. When hylobatids are excluded, differences disappear for SBO (p = 0.246). In BOS, the orthograde catarrhines (hylobatids and humans) are statistically distinguishable from pronograde catarrhines, but hylobatids and humans differ from those pronograde catarrhines in opposite ways (Fig. 4A). In NBO, humans appear to be uniquely derived towards a very flat NBO (Figu.
18 3C). Similarly, in BBT, humans appear to be uniquely derived towards a very short BBT (Fig.
4D). In BCA, where orthograde and pronograde taxa differ significantly, the differences between these groups are so low that they are likely not biologically meaningful (average 0.21 versus
0.20, respectively; Fig. 4E). Among strepsirhines, orthograde and pronograde taxa typically differ significantly from each other, but taxa with mixed locomotor behaviors and those with orthograde behaviors do not. However, there is a great deal of overlap among taxa with different locomotor behaviors and of variation among those with similar behaviors (Figs. 3–4). For example, Hapalemur tends to have a much flatter NBO than Varecia, while Eulemur and Lemur are intermediate, and Otolemur, Euoticus, and Galago tend to have flatter angles than the lorisoids (Fig. 3C). However, this trend is not consistent and does not hold with indriids. The trends in variation that result in significant differences also typically do not hold between strepsirhines and catarrhines.
All PCA results show significant relationships to centroid size and phylogeny (Table 4), in accordance with previous studies (Luboga and Wood, 1990). When both the cranial base and face are included in analyses, size seems to play an important role for primates at all levels.
When compared to the results for the cranial base alone, this suggests that the size of the face is the most important factor driving this relationship. For the cranial base, however, results from the pooled PC1 and centroid size data suggest that the apparent link of size to cranial base morphology is phylogenetic. That is, shape differences occur between genera, and these correspond to size differences between the genera. Among strepsirhines in particular, the small and distinctive lorisoids drive the apparent allometric trend. Allometric trends are also present in
PC2, which separates taxa based on posture and locomotor behavior in geometric morphometrics analyses. Comparing residuals from allometric analyses generally reduces the apparent
19 locomotor trends, especially among catarrhines, where some of the uniqueness of Homo disappears and it appears similar to both Old World Monkeys (PC1 residuals) and hylobatids
(PC2 residuals; see SOM Figs. 7–8). Brain size is only significantly associated with basicranial morphology in catarrhines (Table 4).
Separation between taxa with different locomotor behaviors becomes somewhat clearer when the face is included in geometric morphometrics analyses (Fig. 5). In strepsirrhines, taxa with more positive values along PC1 (lemurids, Otolemur and Galago alleni) have crania with relatively longer faces and palates and more concave foramina magna, while those with more negative values along PC1 (lorisids, Euoticus, Galago senegalensis) have broader crania with shorter faces and palates and more convex foramina magna (Fig. 5A, C). The indriids are intermediate between these two extremes. Along PC2, taxa with more positive values (indriids, lemurids, lorisids) tend to have faces that are oriented along the same axis as the basioccipital, whereas those with more negative values (mainly galagids) tend to have more inferiorly rotated faces and jugular foramina that clearly overlap with the foramen magnum (Fig. 5A, C). PC3 accounts for only 13.58% of variation (SOM Table 4) and tends to separate the indriids and
Hapalemur, a highly orthograde lemurid, from all other strepsirrhines. Taxa with more negative scores along this PC (the indriids and Hapalemur) tend to have shorter faces compared to those with more positive scores (not shown). PC4 does not distinguish between taxa and is not discussed here.
In catarrhines, taxa with more positive values along PC1 (Papio, Macaca mulatta, and hominids, but particularly Homo) tend to have shorter faces, more inferiorly oriented foramina magna, and more extended squamous occipitals, as well as jugular foramina that are more perpendicular relative to the midline (Fig. 5B, D). The external auditory meatus also overlaps
20 with the foramen magnum in the anteroposterior position. Taxa with more negative values along
PC1 (hylobatids and most cercopithecids) tend to have longer faces, more posteriorly oriented foramina magna, and shorter squamous occipitals (Fig. 5B, D). Along PC2, taxa with more positive values (cercopithecoids and hominids except for Homo) tend to have longer faces and palates, with more vertically oriented squamous occipitals (Fig. 5B, D). The external auditory meatus tends to be superior to the basioccipital floor, but overlaps with the foramen magnum in its anteroposterior position. Taxa with more negative values (hylobatids and Homo) tend to have shorter faces and more horizontal squamous occipitals (nuchal planes). The external auditory meatus tends to be anterior to the foramen magnum but ends at the same level as the basioccipital floor. PC3 mainly separates cercopithecoids from hominoids, and taxa overlap completely for PC4, so these and subsequent PCs are not discussed here.
There are significant differences in the morphology of the overall cranium between groups with different locomotor behaviors among strepsirrhines (Pillai = 1.8133, F = 18.479, d.f.
= 236, p < 0.001) and catarrhines, both when Gorilla and Pan are considered pronograde (Pillai
= 0.96898, F = 70.154, d.f. = 146, p < 0.001) and when Gorilla and Pan are considered to display neither orthograde nor pronograde postures (Pillai = 1.9411, F = 74.04, d.f. = 292, p <
0.001). However, 2BPLS indicate that the face and cranial base covary significantly in primates
(Fig. 6A, B). The shape of the cranial base and face is strongly linked to size of the face (p <
0.001; Fig. 6), which may account for the similarity of Indri to non-indriid lemurs (Figs. 1A and
5A). Among primates, bipedal and orthograde taxa tend to have smaller, wider, and less projecting faces than their quadrupedal or pronograde relatives (Fig. 5, Table 5). Among catarrhines in particular, more prognathic faces are associated with more posteriorly oriented foramina magna and less prognathic faces are associated with more inferiorly oriented foramina
21 magna (Fig. 6B). There is some role of brain size in these results among strepsirhines, but the relatively large brains of galagos may drive this relationship (Table 4). The relationship is much stronger among catarrhines and is not driven by Homo, suggesting that brain size is strongly related to both facial and basicranial anatomy: taxa with relatively larger brains tend to have smaller faces that are primarily inferior to the cranial vault rather than primarily anterior to it.
Marsupials
For the cranial base of marsupials, taxa with larger positive values along PC1
(Phascolarctos and the macropods) tend to have transversely narrower squamous occipitals that broaden anteriorly towards the external auditory meatus, which is also superior to the plane of the basioccipital, while taxa with negative values (vombatids) tend to have broader, more square squamous occipitals, with an external auditory meatus that is below the plane of the basioccipital and more convex foramina magna (Fig. 7A, C). Along PC2, taxa with lower values
(Phascolarctos, quadrupedal macropods) tend to have narrower basicrania and the region of the external auditory meatus is at about the same plane as the basioccipital (Fig. 7A, C). Taxa with higher values along PC2 (Lasiorhinus, bipedal macropods) tend to have basicrania that widen towards the external auditory meatus and the region of the external auditory meatus is located superior to the plane of the basioccipital. PC3 largely serves to distinguish Phascolarctos from other marsupials, while PC4 does not show any differences between taxa, so these and subsequent PCs are not discussed here.
Bipedal macropods and orthograde koalas (Phascolarctos) are both differentiated from highly pronograde Vombatus and Lasiorhinus (Fig. 7). However, although pronograde vombatids differ from more orthograde taxa, the morphological differences that are responsible for their
22 separation do not include a more posteriorly oriented foramen magnum (Fig. 7B). To the contrary, vombatids may have the most inferiorly oriented foramina magna of all diprotodonts investigated here. Instead, macropods and koalas differ from vombatids in having narrower crania and more posteriorly oriented foramina magna (Fig. 7C). Further, within macropods, the direction of morphological differences is reversed, so that more quadrupedal macropods such as
Dendrolagus and Potorous converge together, but more closely follow the shape trajectory of orthograde koalas than do bipedal macropods (Bettongia, Macropus, Thylogale). These quadrupedal macropods and koalas tend to display more inferiorly oriented foramina magna and narrower crania than bipedal macropods (Fig. 7C). Orthograde (bipedal macropods and orthograde koalas) and quadrupedal taxa are statistically distinguishable from each other with both CVA (p < 0.0001) and MANOVA (Pillai = 0.67838, F = 15.468, d.f. = 154, p < 0.001), but orthograde koalas are also statistically distinguishable from both quadrupeds and macropod bipeds when orthogrady is treated separately from bipedality in both CVA (p < 0.0001) and
MANOVA (Pillai = 1.562, F = 26.15, d.f. = 308, p < 0.001), and quadrupeds and macropod bipeds actually group together (see SOM Fig. 9).
Like primates, marsupials also display two differing trends in the basion-orbitosphenoid portion of the basicranium. Lasiorhinus and bipedal macropods tend to display a more superior orientation of this segment compared to koalas and quadrupedal macropods, which display a more inferior orientation (Fig. 7C). These differences are likely linked to the unique morphology of the palate, premaxilla, and dentition in each of these taxa.
Among marsupials, significant differences exist between bipeds and quadrupeds only in
SBO and NBO (Table 5, SOM Fig. 11). However, in SBO, bipeds also differ from orthograde koalas, which do not themselves differ from quadrupeds, suggesting that phylogeny plays a
23 strong role in these relationships. All the bipeds are macropods, whereas the majority of the quadrupeds are wombats, which are closely related to koalas. NBO, which is related to the position of the face, may display a stronger signal of positional behavior. Bipedal macropods tend to have lower angles than quadrupeds, and orthograde koalas have lower angles still.
However, this pattern falls apart at the genus level, as Macropus, Phascolarctos, and Vombatus converge in NBO (SOM Table 7).
Size plays a significant role in marsupial cranial base morphology (Table 4). When the allometric component of shape is removed, the majority of taxa group together, although genus- specific differences remain (SOM Fig. 10). Removing size largely removes any apparent postural or locomotor variation.
In a PCA including both basicranial and facial landmarks, the pattern of difference among taxa remains largely the same as with just the basicranium. PC1 primarily represents a separation between macropods on the one hand and the vombatids and Phascolarctos on the other (Fig. 8A). Taxa with negative scores along PC1 (vombatids, Phascolartos) tend to have shorter faces that are oriented on the same plane as the basioccipital plane, as well as squamous occipitals that are relatively wider and more vertical, and external auditory meatuses that are at or inferior to the basioccipital plane (Fig. 8A, B). Taxa with positive scores (macropods) tend to have longer faces that are oriented inferiorly relative to the basioccipital plane, relatively narrower squamous occipitals that are less sharply vertical, and external auditory meatuses that are superior to the basioccipital plane (Fig. 8A, B). In PC2, taxa with more positive scores
(vombatids, most bipedal macropods) tend to have somewhat longer faces and broader basicrania, while those with more negative scores (Phascolarctos, most quadrupedal macropods) tend to have somewhat shorter faces, flatter basioccipitals, and relatively narrower occipitals at
24 asterion (Fig. 8A, C). PC3 primarily separates Macropus and Phascolarctos from other taxa, in which taxa with a more positive score (Macropus and Phascolarctos) tend to have a larger face and taxa with a more negative score tend to have a smaller face (not shown). Most taxa overlap substantially in PC4 and so this and other PCs are not discussed here.
Together, orthograde koalas and macropods tend to have relatively shorter snouts than the quadrupedal wombats (Fig. 8). Interestingly, this relationship is reversed within macropods, so that quadrupedal macropods and Thylogale display shorter snouts than the bipedal macropods
(SOM Table 7). If cranial base morphology is driven by snout length, this explains the apparently contradictory locomotor results when cranial base morphology is analyzed on its own
(Fig. 7). 2BPLS results further indicate that the face and cranial base covary significantly in marsupials (p < 0.001; Fig. 6C). Marsupials with different locomotor behaviors are significantly different from each other when both the cranial base and face are considered using MANOVA, both when koalas are considered separately from bipedal kangaroos (Pillai = 1.8207, F = 39.21, d.f. = 278, p < 0.001) and when they are considered together (Pillai = 0.85108, F = 22.067, d.f. =
139, p < 0.001).
Discussion
Primates
There are subtle changes in primate basicranial morphology associated with locomotor and positional behavior. Orthograde and bipedal taxa typically have somewhat more inferiorly oriented foramina magna than closely related pronograde or quadrupedal taxa, but not more anteriorly positioned foramina magna. Further, among strepsirhines, taxa with mixed locomotor behaviors overlap and converge with more orthograde taxa, suggesting that any amount of
25 orthogrady is morphologically equivalent to obligate orthogrady in the aspects of the cranial base studied here. However, the apparent shifts in cranial base morphology seen in orthograde taxa are tightly linked to changes in the size and position of the face. Orthograde and bipedal taxa not only tend to have more inferiorly oriented foramina magna, they tend to have smaller faces that are less prognathic.
Although platyrrhines are not included here, observations by myself and other authors
(e.g., Le Gros Clark, 1934) suggest that the small-faced platyrrhines such as Cebus and Saimiri converge on the human condition, supporting the hypothesis that it is the face that is driving patterns of change in cranial base morphology. These results are largely in accordance with trends found among primates using two-dimensional data (Bastir et al., 2010) and within modern humans and fossil Homo (Bastir and Rosas, 2016). My results regarding covariation of the face and cranial base also agree with those of Neaux (2017), who found that hominoids display strong covariation of the face and cranial base, and longer more prognathic faces are linked to longer, narrower cranial bases that are oriented more posteriorly.
Muscular changes associated with posture are probably influencing aspects of cranial vault anatomy (Adams and Moore, 1975, Aiello and Dean, 1990, Meyer, 2016). These in turn may influence our interpretations of changes to basicranial anatomy by altering the appearance of the squamous occipital relative to the rest of the cranial base, for example by ‘freeing’ it from the constraints of heavy nuchal attachments and allowing it to extend more posteriorly as in gibbons and humans, especially in the light of brain size changes (Young 1959). However, the size and robusticity of muscle attachment sites are not analyzed here.
Like previous studies using photographic (Ashton and Zuckerman, 1951), radiographic
(Dean and Wood, 1981), or kinematic data (Strait and Ross, 1999), I also conclude that at least
26 some of the perceived variation in foramen magnum anatomy is due to the use of norma basilaris or other standardized views to determine foramen magnum position and distances between landmarks of the cranial base. The use of these standard views obscures aspects of three- dimensional morphology that impact the apparent distances between cranial regions. Further, the use of prosthion-opisthocranion (maximum cranial length), which includes the length of the maxilla, to standardize distances probably obscures the specific role that the face and its relative position play in shaping basicranial morphology.
The dual role of body size, both in directly shaping the morphology of the cranium and in the constraints it places on locomotor behavior, is also likely shaping the apparent locomotor trends in primate basicranial morphology. Size constrains locomotion and posture, so that smaller taxa tend to be vertical clingers and leapers (e.g., among lorisoids) or highly arboreal
(e.g., gibbons), while larger taxa tend to be terrestrial quadrupeds (e.g., among hominoids).
However, part of this relationship is likely due to phylogeny. Among catarrhines, the allometric trend is primarily driven by large-bodied hominoids, which are generally distinctive from both monkeys and gibbons in both size and cranial base shape. Among strepsirrhines, which include taxa of approximately the same size and very different locomotor behavior, the allometric trend is much weaker, again suggesting that phylogeny, rather than strong allometry, plays a significant role. Unfortunately, orangutans are not included in this sample, but observations by this and other authors (e.g., Moore et al., 1973) suggest their basicranial morphology is similar to that of other large-bodied African apes, even though the pattern of integration between their face and basicranial morphology may differ (Senck and Coquerelle, 2015).
The fact that humans display basicranial anatomy more in line with that of smaller taxa is unusual and may be due to our relatively large brain. Relative brain size is not significantly
27 associated with cranial base morphology in strepsirhines, but it plays some role in the morphometric results among catarrhines. These results disagree with those of Ruth et al. (2016), possibly due to the smaller number of taxa used here. These results are, however, consistent with research showing that an increase in the volume of cranial contents influences the shape of the cranial vault to a large degree and of the cranial base to a lesser degree, resulting in some shifts in the apparent angulation and positioning of the foramen magnum (Young, 1959). Phylogeny may again play a role in that hominoids tend to have relatively larger brains than other catarrhines.
This study, which is based on external landmarks of the cranium, does not directly address basicranial flexion, but the results are largely in agreement with those related to the spatial-packing hypothesis. This hypothesis postulates that basicranial flexion is linked to the size of the face and brain (Biegert, 1963; Ross and Ravosa, 1993; Ross and Henneberg, 1995;
Lieberman et al., 2008; Bastir et al., 2010). Relative brain size, as measured in this study, plays a variable role in basicranial morphology, with a stronger role in catarrhines than in strepsirhines, much as in Ross and Ravosa (1993). Like Ross and Ravosa (1993) and Ross and Henneberg
(1995), I also found that orientation of the face is linked to basicranial morphology, and like
Lieberman et al. (2008), Bastir et al. (2010), and Neaux (2017), I find that relatively larger faces are linked to relatively extended and posteriorly oriented cranial bases. However, basicranial flexion is not independently linked to posture (Ross and Ravosa, 1993). It is possible that the general trends observed in this study in regards to locomotion and basicranial morphology in primates are the result of the indirect effects on basicranial morphology of facial and orbital orientation, although these are only loosely and weakly linked to locomotion or posture (Strait and Ross, 1999).
28
Marsupials
Although marsupials were included in the analyses here, they display a different pattern of evolution in basicranial morphology than primates. Despite a general separation between the highly pronograde wombats and a group containing macropods and orthograde koalas, more detailed divisions within the macropods do not support the hypothesis that marsupial basicranial morphology is influenced by locomotion and posture. Specifically, Dendrolagus and Potorous, both pronograde quadrupeds, and Phascolarctos, an orthograde taxon, converge in their basicranial morphology. Dendrolagus and Phascolarctos also converge in aspects of their postcranial skeletal and muscular anatomy, which Grand and Barboza (2001) attribute to their slow-moving arboreality and the propulsive properties and requirements of trees as opposed to soil. It is possible that these same qualities influence marsupial basicranial morphology, although
Potorous is not arboreal. Further, Dendrolagus is thought to have evolved quadrupedalism secondarily from a bipedal ancestor (Windsor and Dagg, 1971), so it is possible that quadrupedal macropods are simply retaining biped-like morphologies from their ancestors and converging with koalas due to those primitive anatomies.
As in primates, at least some of the differences within the macropods are the result of differences in snout length, and it is likely that this also plays a role in basicranial morphology within this closely related group. Together, this suggests that morphological differences of the cranial base are linked to factors other than locomotor or positional behavior.
Implications for the interpretation of the fossil record
29 Although paleoanthropologists typically present the evolution of the craniofacial skeleton as a series of independent changes, it may be more prudent to consider these changes as one interconnected package. Particularly among primates, facial size and projection, as well as position, appear to converge with locomotor behavior, so that orthograde taxa tend to have smaller, less projecting faces and taxa with smaller, less projecting faces tend to have more inferiorly oriented foramina magna. This may have important implications for the interpretation of hominin fossils and the determination of appropriate traits for cladistics analyses.
The various interactions that result in basicranial anatomy mean that the interpretation of fossils requires special caution. A small-bodied, small-faced hominoid may display hominin-like basicranial morphology for reasons unrelated, or only indirectly related, to locomotor behaviors.
Unfortunately, the face is missing in Orrorin (Senut et al., 2001), distorted in
Sahelanthropus (Brunet et al., 2002), and heavily fragmented and reconstructed in Ardipithecus
(Suwa et al., 2009). Regardless, both Sahelanthropus and Ardipithecus are described as having a relatively short mid-face and reduced prognathism relative to chimpanzees, in addition to hominin-like basicranial features including a more inferior and anterior foramen magnum
(Brunet et al., 2002; Zollikofer et al., 2005; Suwa et al., 2009). While Sahelanthropus has reduced prognathism relative to Australopithecus and Homo, and Ardipithecus has a somewhat more projecting face than both taxa, these early hominins tend towards a smaller-face, reduced- prognathism condition compared to chimpanzees (Brunet et al., 2002; Zollikofer et al., 2005;
Suwa et al., 2009). There are no crania of Australopithecus anamensis, the earliest australopith, that are complete enough to discuss facial length or orientation. However, although one of the more complete skulls of Australopithecus afarensis, AL-444, is heavily reconstructed, it has also
30 been described as displaying substantially reduced prognathism relative to chimpanzees (Kimbel et al., 2004).
Putative early hominins are also typically estimated to have low body masses, with
Orrorin and Ardipithecus estimated at 35.8 kg and 32.1 kg, respectively, and early
Australopithecus anamensis estimated at 46.3 kg (Grabowski et al., 2015). These estimates fall within those of Pan paniscus (mass 33.2–45 kg; Fleagle 2013), which has a more inferiorly oriented foramen magnum and posteriorly extended squamous occipital than larger non-human hominoids, despite locomotor similarities to those larger hominoids.
Further, brain size plays a role in basicranial anatomy among catarrhines and early hominins that fall within hylobatid-Homo ranges for relative brain size. Estimates of brain to body mass ratios for Australopithecus africanus, for example, range from 0.016 (for STS71;
Kappelman, 1996) to 0.017 (for STS 5; Kappelman, 1996), which falls within the estimates for
Hoolock (0.016) and Hylobates (0.017) and are very different than estimates of either Pan
(0.008–0.009) or Gorilla (0.003–0.006). If Sahelanthropus tchadensis had a brain of 365 cm3
(Zollikofer et al., 2005), and a body mass similar to that of other very early hominins ranging between 32.1 kg and 35.8 kg (Grabowski et al., 2015), its approximate brain to body mass ratio would be 0.010–0.011. This range is close to Pan paniscus (0.009) and also to Symphalangus
(0.010). The cranial base of Sahelanthropus thus could be expected to resemble that of bonobos or hylobatids, which are more similar to Homo than chimpanzees are, simply because of body and brain size.
Some traits related to foramen magnum position and orientation do vary between humans and other hominoids, as reported in previous literature (e.g., Tobias, 1967; Luboga and Wood,
1990; Kimbel and Rak, 2010; Russo and Kirk, 2013), so that humans tend to have shorter
31 sphenooccipital regions than other hominoids and a shift in the relative position of the temporal bones, but these differences are unlikely to be related to locomotion. Hence, fossils like
Paranthropus aethiopicus specimen KNM-WT 17000 or Paranthropus boisei specimen KNM-
ER 406 display a very shortened spheno-occipital region, but otherwise retain a foramen magnum orientation similar to that of Pan. Although this shortening may serve as a trait for cladistics analyses, it should not be used to indicate whether a particular fossil was bipedal.
Further, despite generalized trends linked to positional or locomotor behavior and to overall and facial size, there is also substantial overlap between taxa, which may be due to factors such as size or to more nuanced variation in positional and locomotor behavior than is possible to test here (e.g., Strait and Ross, 1999). As a result of this substantial variation, it is unlikely that individual specimens will display interpretable morphology unless they fall into the extremes occupied by taxa such as Homo or the Hylobatidae.
Conclusion
The ability to infer locomotor pattern from basicranial morphology is complicated by the multiple interactions between the face, brain, and body size. Primate patterns of basicranial morphology linked to locomotion and posture are not conserved across mammals. Miocene hominoids, including early hominins, may display inferiorly oriented foramina magna regardless of their locomotor behavior, and a shift towards an anterior position of the foramen magnum may represent a phylogenetic rather than functional trait. Further investigation into how craniofacial anatomy and head carriage are affected by posture, locomotion, speed, and substrate will clarify these interactions. These results also highlight the utility of using three-dimensional data when possible.
32
33 Acknowledgments
I would like to thank Susan C. Antón, Terry Harrison, Scott Williams, Emily Middleton, and three anonymous reviewers for helpful comments throughout the preparation of this manuscript. I would also like to thank Eileen Westwig at the American Museum of Natural
History; William Stanley and Rebecca Banasiak at the Field Museum; Judith Chupasko and
Mark Omura at the Harvard Museum for Comparative Zoology; Mark Carnall at the Oxford
Museum of Natural History; Hellen Opolot at the Uganda National Council for Science and
Technology; Peace, Masili Godfrey, Duncan Kange, Jackson Batte, and Drs. William Buwembo and Erisa Mwaka at Makerere College; Brendon Billings, Jason Hemingway, and Daigo
Shangase at the University of Witwatersrand; Christiane Funk at the Museum für Naturkunde;
Katrin Krohmann at the Senckenberg Instiute; Drs. Géraldine Veron, Christiane Denys, and
Jacques Cuisin at the Musée National d’Histoire Naturelle; Pepijn Kamminga at the Naturalis
Biodiversity Center; Terry Walschaerts, Karine Maurice, and Drs. Patrick Semal and Georges
Lenglet, at the Royal Belgian Institute of Natural Sciences; Emmanuel Gilissen and Wim
Wendelen at the Royal Museum of Central Africa; Roberto Portela Miguez at the Natural
History Museum in London; Dr. Inbal Livne at the Powell-Cotton Museum; Dr. Daniel Antoine at the British Museum; and all others who helped with access to collections.
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42 Figures
Figure 1. Geometric morphometric comparisons of the basicranium among strepsirhines. A) Genus-specific convex hulls; B) taxon means mapped onto a phylogeny, color-coded by locomotor behavior (dark blue = pronograde quadruped, light blue = antipronograde, pink = vertical clinger and leaper, green = mixed); C) lateral and inferior views of shape variation associated with PC1 and PC2. The red line in the lateral view of 1C highlights the orientation of the foramen magnum, while the black line highlights the basion-sphenobasion-orbitosphenoid angle discussed in the text.
43
Figure 2. Geometric morphometric comparisons of the basicranium among catarrhines. A) Taxon-specific convex hulls; B) taxon means mapped onto a phylogeny, color-coded by locomotor behavior (dark blue = pronograde quadruped, purple = orthograde quadruped, red = orthograde suspensory, orange = orthograde biped); C) lateral and inferior views of shape variation associated with PC1 and PC2. The red line in the lateral view of 1C highlights the orientation of the foramen magnum, while the black line highlights the basion-sphenobasion- orbitosphenoid angle discussed in the text.
44
Figure 3. Boxplots showing the mean and range for cranial base angles of primates. A) SBO angle by genus, B) PBO angle by genus, C) NBO by genus. Key: Nyct = Nycticebus, Prdc = Perodicticus, Galg = Euoticus and Galago, Elmr = Eulemur, Hplm = Hapalemur, Lemur = Lemur, Varc = Varecia, Avah = Avahi, Indr = Indri, Prpt = Propithecus, Crcp = Chlorocebus, Macc = Macaca, Papi = Papio, Hlck = Hoolock, Hylb = Hylobates, Symp = Symphalangus, GrlM = Gorilla male, GrlF = Gorilla female, Pnpn = Pan paniscus, Pntr = Pan troglodytes, Homo = Homo. Colors are as follows: in strepsirrhines, yellow = quadrupedal, red = vertical clinger and leaper, pink = mixed locomotion; in catarrhines, blue = quadrupedal, light green = orthograde suspensory, dark green = bipedal.
45
Figure 4. Boxplots showing the mean and range for cranial measurements of primates. A) Relative BOS by genus, B) relative BSB by genus, C) relative SBB by genus, D) relative BBT by genus, E) relative BCA by genus. Key: Nyct = Nycticebus, Prdc = Perodicticus, Galg = Euoticus and Galago, Elmr = Eulemur, Hplm = Hapalemur, Lemur = Lemur, Varc = Varecia, Avah = Avahi, Indr = Indri, Prpt = Propithecus, Crcp = Chlorocebus, Macc = Macaca, Papi = Papio, Hlck = Hoolock, Hylb = Hylobates, Symp = Symphalangus, GrlM = Gorilla male, GrlF = Gorilla female, Pnpn = Pan paniscus, Pntr = Pan troglodytes, Homo = Homo. Colors are as follows: in strepsirrhines, yellow = quadrupedal, red = vertical clinger and leaper, pink = mixed locomotion; in catarrhines, blue = quadrupedal, light green = orthograde suspensory, dark green = bipedal.
46
Figure 5. Geometric morphometric comparisons of the combined face and basicranium in primates. A) Taxon means of strepsirhine face and basicranial morphology mapped onto a phylogeny, B) taxon means of catarrhine face and basicranial morphology mapped onto a phylogeny, C) shape changes associated with PC1 and PC2 among strepsirhine taxa, D) shape changes associated with PC1 and PC2 among catarrhine taxa. In both A and B, colors indicate locomotor category as follows dark blue = pronograde quadruped, light blue = antipronograde, pink = vertical clinger and leaper, green = mixed.
47
Figure 6. 2B-PLS shape covariation results for the face and basicranium from PLS1. A) Shape relationships between the face and basicranium among strepsirrhines (PLS1 = 69.4% total covariation, RV = 0.5652, p < 0.001), B) shape relationships between the face and basicranium among catarrhines (PLS1 = 55.6% total covariation, RV = 0.5246, p < 0.001), C) shape relationships between the face and basicranium among diprotodonts (PLS1 = 63.2% total covariation, RV = 0.3235, p < 0.001). The facial module is marked by black landmarks and the basicranial module by red landmarks.
48 Figure 7. Geometric morphometric comparisons of the basicranium among diprotodonts. A) Genus-specific convex hulls, B) taxon means mapped onto a phylogeny (dark blue = pronograde quadruped, purple = orthograde, dark orange = pronograde biped), C) lateral and inferior views of shape variation associated with PC1 and PC2. The additional line in the lateral view of 1C highlights the orientation of the foramen magnum.
49
Figure 8. Geometric morphometric comparisons of the combined face and basicranium in diprotodonts. A) Taxon means mapped onto a phylogeny, B) shape changes associated with PC1, C) shape changes associated with PC2. In B, colors indicate locomotor category as follows: dark blue = pronograde quadruped, purple = orthograde, dark orange = pronograde biped.
50 Tables
Table 1. Primate sample.
Order Suborder Family Species N Posture Source Primates Catarrhini Cercopithecidae Chlorocebus pygerythrus 20 Pronograde Quadruped Fleagle (2013) Macaca fascicularis 25 Pronograde Quadruped Fleagle (2013) Macaca mulatta 10 Pronograde Quadruped Fleagle (2013) Papio hamadryas 8 Pronograde Quadruped Fleagle (2013) Hominidae Gorilla gorilla 24 Orthograde Quadruped Fleagle (2013) Homo sapiens 32 Orthograde Biped - Pan paniscus 25 Orthograde Quadruped Fleagle (2013) Pan troglodytes 27 Orthograde Quadruped Fleagle (2013) Hylobatidae Hoolock hoolock 25 Orthograde Suspensory Fleagle (2013) Hylobates lar 25 Orthograde Suspensory Fleagle (2013) Symphalangus syndactylus 29 Orthograde Suspensory Fleagle (2013) Total 250 Strepsirhini Galagidae Euoticus elegantulus 26 Vertical Clinger and Leaper Crompton (1984), Fleagle (2013) Galago alleni 1 Vertical Clinger and Leaper Crompton (1984) Galago senegalensis 2 Vertical Clinger and Leaper Crompton (1984), Gebo (1987) Otolemur crassicaudatus 28 Mixed Bearder and Doyle (1974), Crompton (1984) Indriidae Avahi laniger 4 Vertical Clinger and Leaper Shapiro and Simons (2002) Indri indri 6 Vertical Clinger and Leaper Shapiro and Simons (2002) Propithecus sp. 26 Vertical Clinger and Leaper Gebo (1987) Lemuridae Eulemur sp. 27 Mixed Gebo (1987), Shapiro and Simons (2002) Hapalemur griseus 14 Vertical Clinger and Leaper Gebo (1987), Shapiro and Simons (2002) Lemur catta 9 Pronograde Quadruped Gebo (1987) Varecia variegata 27 Pronograde Quadruped Gebo (1987), Shapiro and Simons (2002) Lorisidae Nycticebus sp. 27 Antipronograde Quadruped Walker (1969), Gebo (1987), Shapiro and Simons (2002) Perodicticus potto 26 Antipronograde Quadruped Walker (1969), Gebo (1987), Shapiro and Simons (2002) Total 223
51 Table 2. Marsupial sample.
Order Suborder Family Species N Posture Source Diprotodontia Macropodiformes Macropodidae Dendrolagus benettianus 6 Pronograde Quadruped Windsor and Dagg (1971) Dendrolagus inustus 15 Pronograde Quadruped Procter-Gray and Ganslosser (1986) Dendrolagus lumholtzi 17 Pronograde Quadruped Procter-Gray and Ganslosser (1986) Macropus agilis 7 Pronograde Biped Windsor and Dagg (1971) Macropus giganteus 6 Pronograde Biped Windsor and Dagg (1971) Macropus parma 7 Pronograde Biped Windsor and Dagg (1971) Macropus robustus 16 Pronograde Biped Windsor and Dagg (1971) Macropus rufogriseus 14 Pronograde Biped Windsor and Dagg (1971) Macropus rufus 6 Pronograde Biped Windsor and Dagg (1971) Thylogale billardieri 3 Pronograde Biped Windsor and Dagg (1971) Thylogale brunii 3 Pronograde Biped Windsor and Dagg (1971) Thylogale stigmatica 6 Pronograde Biped Windsor and Dagg (1971) Potoroidae Bettongia lesueur 17 Pronograde Biped Webster and Dawson (2003) Bettongia penicillata 12 Pronograde Biped Webster and Dawson (2003) Potorous tridactylus 28 Pronograde Quadruped Baudinette et al. (1993) Vombatiformes Phascolarctidae Phascolarctos cinereus 29 Orthograde Quadruped Grand and Barboza (2001) Vombatidae Lasiorhinus latifrons 11 Pronograde Quadruped Grand and Barboza (2001) Vombatus ursinus 28 Pronograde Quadruped Grand and Barboza (2001) Total 231
52 Table 3. Linear and angular measurements of the cranium.a Measurement Abbreviation Type Basion to sphenobasion BSB Linear Basion to orbitosphenoid BOS Linear Basion to midpoint of a line running through the anteriormost point of both carotid canalsb BCA Linear Basion to midpoint of bitympanic linec BBT Linear Sphenobasion breadth SBB Linear Nasion to prosthion NAP Linear Prosthion to the posterior palate PPP Linear Palate breadth PBR Linear Sphenobasion-basion-opisthion SBO Angular Nasion-basion-opisthion NBO Angular Posterior palate-basion-opisthion PBO Angular aLinear measurements are analyzed as indices relative to the nasion-opisthocranion length, except for SBB, which is taken relative to BSB length, and PBR, which is taken relative to PPP. bCalculated only for catarrhines cCalculated only for primates
53 Table 4. Regression results.a
PC1 Size – Ungrouped PC1 Size – Grouped PC2 Size – Ungrouped PC2 Size - Grouped N R2 p-value R2 p-value R2 p-value R2 p-value Cranial base and face Strepsirhines 0.4771 < 0.0001 0.2314 < 0.0001 180 0.3786 < 0.0001 0.0762 0.0002 Lemuroidea 0.3605 < 0.0001 - - 86 0.5881 < 0.0001 - - Lorisoidea 0.0024 0.6425 - - 94 0.3786 < 0.0001 - - Catarrhines 0.1765 < 0.0001 0.3636 < 0.0001 212 0.2429 < 0.0001 0.3483 < 0.0001 Cercopithecoids 0.0204 0.3124 - - 52 0.8706 < 0.0001 - - Hominoids – with Homo 0.1726 < 0.0001 - - 212 0.2393 < 0.0001 - - Hominoids – without Homo 0.2684 < 0.0001 - - 138 0.9350 < 0.0001 - - Diprotodontia 0.0004 0.7885 0.0140 0.1184 176 0.0001 < 0.8640 0.0032 0.4588 Cranial base only Strepsirhines 0.4362 < 0.0001 0.0129 0.1097 200 0.2312 < 0.0001 0.0011 0.6425 Lemuroidea 0.0981 0.0020 - - 95 0.1409 0.0002 - - Lorisoidea 0.0000 0.9683 - - 105 0.5286 < 0.0001 - - Catarrhines 0.2029 < 0.0001 0.0005 0.7441 232 0.0230 0.0207 0.0872 < 0.0001 Cercopithecoids 0.5220 < 0.0001 - - 57 0.3040 < 0.0001 - - Hominoids – with Homo 0.1555 < 0.0001 - - 234 -0.0030 0.5193 Hominoids – without Homo 0.7003 < 0.0001 - - 145 0.6691 < 0.0001 - - Diprotodontia 0.4305 < 0.0001 0.1183 < 0.0001 176 0.1774 < 0.0001 0.1709 < 0.0001 Phylogeny PC1 Brain Size PC2 Brain Size p-value R2 p-value R2 p-value Cranial base and face Strepsirhines 0.0002 0.0499 0.5091 0.4435 0.0253 Catarrhines 0.0032 0.0600 0.4429 0.6287 0.0021 Diprotodontia < 0.0001 0.1289 0.1887 0.0126 0.6902 Cranial base only Strepsirhines < 0.0001 0.2200 0.1456 0.1491 0.2408 Catarrhines 0.0003 0.0004 0.9508 0.4713 0.0137 Diprotodontia < 0.0001 0.0754 0.3220 0.0062 0.7796 aResiduals are plotted in SOM Figures 5–7.
54 Table 5. Significance values for all comparisons of linear and angular measurements. SBO PBO NBO BOS BSB SBB BBT BCA NAP PPP PBR Strepsirhines Orthograde-Pronograde + + + + + + - NA + + + Orthograde-Antipronograde - + + + + - + NA - - + Orthograde-Mixed - - - - - + - NA + + - Pronograde-Antipronograde + - - + + + + NA + + + Pronograde-Mixed + + + + + - - NA + + + Mixed-Antipronograde - + + + + + + NA + + + Catarrhines Orthograde-Pronograde + + - + - + + + + + + Diprotodontia Bipedal-Orthograde + - + - - - NA NA + + + Bipedal-Quadrupedal + - + - - - NA NA + + + Orthograde-Quadrupedal ------NA NA + + + + indicates a significant difference, - indicates no significant difference. More detailed information, including means and standard deviations, is provided in SOM Tables 5–7 and the marsupial ranges are provided in SOM Figure 11.
55
SOM Figure 1. Phylogenetic tree used for strepsirhines, based on data from 10kTrees Version 3.0 (Arnold et al., 2010). Color key: dark blue = pronograde quadruped, light blue = antipronograde, pink = vertical clinger and leaper, green = mixed.
SOM Figure 2. Phylogenetic used for catarrhines, based on data from 10kTrees Version 3.0 (Arnold et al., 2010). Color key: dark blue = pronograde quadruped, purple = orthograde quadruped, red = orthograde suspensory, orange = orthograde biped.
SOM Figure 3. Phylogenetic tree used for diprotodont marsupials, based on the data provided in Cardillo et al. (2004) and Meredith et al. (2008, 2009). Color key: dark blue = pronograde quadruped, light purple = orthograde, dark orange = pronograde biped.
SOM Figure 4. Landmarks collected on the cranium, shown on inferior view of Otolemur cranium. Numbers correspond to numbers in SOM Table 1. Nasion and the lateral nasal landmarks are not shown here because they are not visible from an inferior view. The carotid canal is not shown here, as this was only collected on catarrhines.
SOM Figure 5. CVA results for strepsirhine cranial base shape. Orthograde (bipedal or otherwise) taxa include: Homo, Hoolock, Hylobates, and Symphalangus. Pronograde/quadrupedal taxa include: Chlorocebus, Gorilla, Macaca, Pan, and Papio.
SOM Figure 6. CVA results for catarrhine cranial base shape. Orthograde (bipedal or otherwise) taxa include: Homo, Hoolock, Hylobates, and Symphalangus. Pronograde/quadrupedal taxa include: Chlorocebus, Gorilla, Macaca, Pan, and Papio.
SOM Figure 7. Plot of the cranial base residuals from allometric analyses for strepsirhines. Orthograde (bipedal or otherwise) taxa include: Homo, Hoolock, Hylobates, and Symphalangus. Pronograde/quadrupedal taxa include: Chlorocebus, Gorilla, Macaca, Pan, and Papio.
SOM Figure 8. Plot of the cranial base residuals from allometric analyses for catarrhines. Orthograde (bipedal or otherwise) taxa include: Homo, Hoolock, Hylobates, and Symphalangus. Pronograde/quadrupedal taxa include: Chlorocebus, Gorilla, Macaca, Pan, and Papio.
SOM Figure 9. CVA results for diprotodont marsupial cranial base shape, using all three locomotor categorizations. Bipedal taxa include: Bettongia, Macropus, and Thylogale. Orthograde taxa include: Phascolaractos. Quadrupedal taxa include: Dendrolagus, Lasiorhinus, Potorous, and Vombatus.
SOM Figure 10. Plot of the cranial base residuals from allometric analyses for diprotodont marsupials. Bipedal taxa include: Bettongia, Macropus, and Thylogale. Orthograde taxa include: Phascolaractos. Quadrupedal taxa include: Dendrolagus, Lasiorhinus, Potorous, and Vombatus.
SOM Figure 11. Angles and measurements of diprotodont marsupials. Lsrh = Lasiorhinus, Vmbt = Vombatus, Phsc = Phascolarctos, Bttn = Bettongia, Ptrs = Potorous, Dndr = Dendrolagus, Mcrp = Macropus, Thyl = Thylogale. Color-coded by locomotion: yellow = quadrupedal, purple = orthograde, blue = bipedal. SOM Table 1. List and description of landmarks use in this study. An image of the landmarks is available in SOM Figure 4. Number Name Description 1 Nasion Point where the right and left nasal bones meet the frontal 2 R, L Lateral nasal Most lateral point on the suture between the frontal and nasal bones 3 Prosthion Most anterior midline point on the maxillae 4 R, L Premaxilla Point where premaxillary suture meets the edge of the palate or, when the suture is not visible, point at the edge of the palate between the lateral incisor and the canine 5 Incision Midline point on the most posterior edge of the incisive foramen or, when the foramen is irregularly shaped, point where a line tangent to the most posterior edge of the foramen and perpendicular to the midline meets the midline 6 R, L Maximum palate Point on the alveolar bone laterally, just above the tooth row, where the breadth greatest breadth of the palate occurs 7 R, L Ectomolare Point on the alveolar bone laterally, just above the midpoint of the last molar of the tooth row 8 Posterior palate Most posterior point on the palate 9 R, L Zygomatic Most inferior point on zygomatico-temporal suture 10 R, L Lateral GF Most lateral on the articular surface of the glenoid fossa 11 R, L Medial GF Most medial point on the articular surface of the glenoid fossa 12 R, L Auriculare In primates only, most superior point on the edge of the external auditory meatus 13 R, L Posterior EAM In primates only, most posterior point on the edge of the external auditory meatus 14 R, L Inferior EAM In primates only, most inferior point on the edge of the external auditory meatus 15 R, L Carotid canal In catarrhines only, most medial point on the edge of the carotid canal 16 Sphenobasion Midline point on the sphenooccipital suture 17 R, L Lateral Most lateral point on the sphenooccipital suture, taken on the edge where sphenobasion the curvature of the bone shifts 18 Orbitosphenoid In diprotodonts and strepsirhines, midline point on the suture between the orbitosphenoid and basisphenoid; in catarrhines, midline point along the posterior edge of vomer 19 R, L Medial jugular Most medial point on the edge of the jugular canal, typically where the temporal (petrosal) and occipital bones meet 20 R, L Lateral jugular Most lateral point on the edge of the jugular canal, typically where the temporal (petrosal) and occipital bones meet 21 R, L Petrous temporal In primates only, most anterior, medial point on the petrous portion of the temporal bone 22 Basion Most anterior point on edge of foramen magnum 23 R, L Lateral FM Most lateral point on foramen magnum, occurring outside the region of overlap with the occipital condyles 24 Opisthion Most posterior point on edge of foramen magnum 25 Opisthocranion Midline point on the occipital where the distance between prosthion and the occipital is greatest; in catarrhines, where the distance between glabella and the occipital is greatest 26 R, L Asterion In diprotodonts, point where the parietal, supraoccipital, and exocciptal meet; in primates, point where the lambdoidal and squamosal sutures meet SOM Table 2. Brain volumes and body masses for primates. * indicates that data were reported as brain mass and were converted to volume using the equation provided in Stephan et al., (1981). When more than one volume is listed, an average was used for analyses. Brain Volume Body Mass (g) Citation (mm3) Strepsirhines Nycticebus coucang 11755 800 Stephan et al., 1981 Perodicticus potto 13212 1150 Stephan et al., 1981
Euoticus elegantulus 6950* 274 Leonard et al., 2003 Galago senegalensis 4512 186 Stephan et al., 1981
Otolemur crassicaudatus 9668 850 Stephan et al., 1981 Eulemur fulvus 22106 1400 Stephan et al., 1981 Hapalemur griseus 14093* 709 MacLean et al., 2009 Lemur catta 2210 Leonard et al., 2003; MacLean et 22905* 2678 al., 2009 Varecia variegata 29713 3000 Stephan et al., 1981; MacLean et 32124* 3599 al., 2009 Avahi laniger 9798 1285 Stephan et al., 1981; MacLean et 9865* 1207 al., 2009 Indri indri 36285 6250 Stephan et al., 1981; MacLean et 34807 * 6335 al., 2009 Propithecus verreauxi 25194 3480 Stephan et al., 1981; MacLean et 26207* 2955 al., 2009 Catarrhines Cercopithecus mitis 70564 6300 Stephan et al., 1981; Leonard et 73359* 6500 al., 2003 Macaca fascicularis 71429* 5500 Leonard et al., 2003 Macaca mulatta 87896 7800 Stephan et al., 1981 Papio anubis 166400 23520 Kappelman 1996 141400 11860 Papio ursinus 183398* 18000 Leonard et al., 2003 Hoolock hoolock 108000 6930 Kappelman 1996 100200 6480 Hylobates lar 97505 5700 Stephan et al., 1981 Symphalangus syndactylus 111800 10900 Kappelman 1996 113200 10600 Gorilla gorilla (M) 537500 169500 Kappelman 1996 Gorilla gorilla (F) 441400 71500 Kappelman 1996 Pan paniscus 295500 33200 Kappelman 1996 Pan troglodytes 382103 46000 Stephan et al., 1981 Homo sapiens 1251847 65000 Stephan et al., 1981
SOM Table 3. Brain volumes and body masses for diprotodonts (marsupials) from Isler (2011). No brain volume estimates were available for Potorous tridactylus. Brain Volume (mm3) Body Mass (g) Lasiorhinus latifrons 55500 26000 Vombatus ursinus 59000 26000 Phascolarctos cinereus 20200 5100 Bettongia lesueur 10500 1300 Bettongia penicillata 9560 1300 Potorous tridactylus - - Dendrolagus bennettianus 18500 9300 Dendrolagus inustus 30100 11400 Dendrolagus lumholtzi 26200 6475 Macropus agilis 33300 11000 Macropus giganteus 69800 17800 Macropus parma 18700 3550 Macropus robustus 59000 15600 Macropus rufogriseus 36000 13800 Macropus rufus 62400 26500 Thylogale stigmatica 17800 3800
SOM Table 4. Eigenvalues and percent variance for PC scores. Only the first four PC scores are shown because in no case did PC5 or higher account for more than 5% of the variance. Strepsirhines Catarrhines Diprotodontia Eigenvalues % Variance Eigenvalues % Variance Eigenvalues % Variance Face and Cranial Base PC1 0.00343001 35.888 0.00496488 35.36 0.00332662 35.004 PC2 0.00203758 21.319 0.00416335 29.651 0.0020528 21.6 PC3 0.00129826 13.584 0.00147609 10.513 0.00149933 15.776 PC4 0.0004952 5.181 0.00062578 4.457 0.00069891 7.354 Cranial Base Only PC1 0.0051554 38.451 0.00457084 30.984 0.0081397 43.264 PC2 0.00240911 17.968 0.00355392 24.091 0.00347379 18.464 PC3 0.00143653 10.714 0.00175125 11.871 0.00232129 12.338 PC4 0.0006937 5.174 0.00108995 7.388 0.00125012 6.645
SOM Table 5. Means and standard deviations for the angles calculated for primates. Measured in degrees. SBO SD PBO SD NBO SD Strepsirhines Nycticebus 132.16 6.28 138.45 5.72 121.83 5.71 Perodicticus 123.37 7.01 126.82 6.99 109.25 6.67 Euoticus and Galago 129.08 5.70 144.22 4.73 132.90 3.32 Otolemur 128.92 5.06 144.22 4.71 126.23 3.86 Eulemur 129.43 5.38 142.00 4.59 124.48 4.25 Hapalemur 137.85 5.96 149.66 5.03 135.01 5.91 Lemur 129.37 3.36 141.67 2.79 124.20 2.71 Varecia 118.77 6.09 131.12 5.84 114.03 5.03 Avahi 127.21 7.59 141.35 5.48 128.00 6.65 Indri 120.40 3.91 133.50 1.41 113.07 1.02 Propithecus 125.66 4.94 142.04 4.66 122.14 4.62 Locomotion Orthograde 128.34 7.07 143.17 4.98 127.53 8.09 Pronograde 120.82 7.05 133.16 6.82 116.00 6.18 Antipronograde 127.77 7.94 132.64 8.63 115.54 8.84 Mixed 129.18 5.17 143.11 4.73 125.36 4.11 T-test p-value O-P < 0.0001 < 0.0001 < 0.0001 T-test p-value O-A 0.9703 < 0.0001 < 0.0001 T-test p-value O-M 0.9182 1.000 0.3859 T-test p-value P-M < 0.0001 < 0.0001 < 0.0001 T-test p-value P-A 0.0001 0.9858 0.9925 T-test p-value M-A 0.7437 < 0.0001 < 0.0001 Catarrhines Chlorocebus 152.36 5.46 160.83 4.47 132.06 4.65 Macaca 151.88 6.80 162.78 6.47 134.64 7.26 Papio 145.33 7.40 169.04 8.73 125.80 5.98 Hoolock 142.78 4.68 149.83 3.89 126.99 3.14 Hylobates 140.62 4.49 153.09 3.88 128.04 3.52 Symphalangus 140.60 5.20 150.09 5.58 126.10 5.74 Gorilla (M) 148.89 9.45 165.12 7.96 122.73 8.42 Gorilla (F) 149.64 9.91 170.23 3.69 128.86 5.92 Pan paniscus 153.71 5.57 174.69 3.32 136.98 4.26 Pan troglodytes 155.05 5.03 171.04 4.90 133.45 4.55 Homo 153.59 5.58 170.70 5.38 157.09 4.61 Locomotion Orthograde 144.10 7.20 155.56 9.7 134.01 13.53 Pronograde 152.00 7.06 167.49 7.37 132.48 7.02 T-test p-value < 0.0001 < 0.0001 0.2980
SOM Table 6. Means and standard deviations for the measurements calculated for primates. All measurements are provided as proportions of NOC, except SBB, which is provided as a proportion of BSB, and PBR, which is provided as a proportion of PPP. BOS SD BSB SD SBB SD BBT SD BCA SD Strepsirhines Nycticebus 0.40 0.04 0.22 0.03 0.51 0.09 0.61 0.03 - Perodicticus 0.45 0.02 0.25 0.03 0.42 0.08 0.54 0.05 - Euoticus and Galago 0.32 0.02 0.17 0.02 0.43 0.07 0.44 0.02 - Otolemur 0.35 0.02 0.19 0.02 0.57 0.07 0.45 0.02 - Eulemur 0.36 0.04 0.21 0.02 0.54 0.08 0.39 0.02 - Hapalemur 0.36 0.03 0.20 0.01 0.47 0.12 0.40 0.02 - Lemur 0.39 0.01 0.19 0.02 0.55 0.07 0.42 0.01 - Varecia 0.40 0.02 0.23 0.02 0.52 0.05 0.41 0.02 - Avahi 0.34 0.03 0.18 0.01 0.52 0.04 0.40 0.01 - Indri 0.44 0.03 0.25 0.01 0.50 0.06 0.45 0.03 - Propithecus 0.38 0.03 0.22 0.02 0.52 0.06 0.44 0.05 - Locomotion Orthograde 0.36 0.05 0.20 0.03 0.48 0.09 0.43 0.03 - Pronograde 0.40 0.02 0.22 0.02 0.52 0.06 0.42 0.02 - Antipronograde 0.42 0.04 0.24 0.03 0.47 0.09 0.57 0.05 Mixed 0.35 0.04 0.20 0.02 0.56 0.07 0.42 0.04 - Tukey’s p-value O-P < 0.0001 0.0014 0.0425 0.1396 - Tukey’s p-value O-A < 0.0001 < 0.0001 0.9458 < 0.0001 - Tukey’s p-value O-M 0.9458 0.9681 < 0.0001 0.3430 - Tukey’s p-value P-A 0.0309 0.0313 0.0174 < 0.0001 - Tukey’s p-value P-M < 0.0001 0.0008 0.2668 0.9206 - Tukey’s p-value M-A < 0.0001 < 0.0001 < 0.0001 < 0.0001 - Catarrhines Chlorocebus 0.27 0.02 0.16 0.01 0.72 0.07 0.51 0.03 0.19 0.01 Macaca 0.29 0.02 0.16 0.02 0.74 0.10 0.52 0.02 0.19 0.01 Papio 0.28 0.02 0.18 0.03 0.77 0.07 0.57 0.02 0.22 0.01 Hoolock 0.38 0.02 0.19 0.01 0.65 0.07 0.55 0.01 0.21 0.01 Hylobates 0.35 0.03 0.19 0.01 0.63 0.08 0.61 0.02 0.21 0.02 Symphalangus 0.43 0.02 0.21 0.02 0.61 0.08 0.57 0.02 0.20 0.02 Gorilla (M) 0.29 0.02 0.21 0.02 0.62 0.09 0.61 0.03 0.22 0.01 Gorilla (F) 0.28 0.02 0.20 0.01 0.62 0.07 0.59 0.04 0.22 0.02 Pan paniscus 0.30 0.02 0.20 0.02 0.70 0.10 0.61 0.02 0.19 0.02 Pan troglodytes 0.29 0.02 0.20 0.02 0.68 0.10 0.61 0.03 0.22 0.02 Homo 0.17 0.01 0.14 0.01 0.84 0.08 0.45 0.02 0.21 0.01 Locomotion Orthograde 0.34 0.10 0.19 0.03 0.68 0.12 0.54 0.06 0.21 0.02 Pronograde 0.29 0.02 0.18 0.03 0.70 0.10 0.57 0.05 0.20 0.02 T-test p-value < 0.0001 0.2658 0.0441 0.0008 0.0047 T-test T 5.06 1.12 -2.02 -3.40 2.86 Degrees of freedom 109.31 212.35 200.74 212.88 222.61
SOM Table 6 (cont). NAP SD PPP SD PBR SD Strepsirhines Nycticebus 0.46 0.04 0.51 0.03 0.92 0.05 Perodicticus 0.41 0.04 0.48 0.02 1.02 0.06 Euoticus and Galago 0.39 0.04 0.47 0.02 0.86 0.05 Otolemur 0.52 0.06 0.55 0.03 0.91 0.03 Eulemur 0.52 0.04 0.60 0.03 0.75 0.04 Hapalemur 0.43 0.03 0.49 0.01 0.87 0.07 Lemur 0.50 0.02 0.56 0.01 0.83 0.03 Varecia 0.60 0.04 0.68 0.03 0.73 0.03 Avahi 0.36 0.02 0.43 0.02 1.02 0.05 Indri 0.56 0.06 0.52 0.04 0.96 0.07 Propithecus 0.43 0.04 0.48 0.03 0.98 0.06 Locomotion Orthograde 0.45 0.07 0.51 0.06 0.87 0.11 Pronograde 0.59 0.05 0.66 0.05 0.75 0.05 Antipronograde 0.43 0.04 0.50 0.03 0.97 0.07 Mixed 0.52 0.06 0.55 0.03 0.91 0.03 Tukey’s p-value O-P < 0.0001 < 0.0001 < 0.0001 Tukey’s p-value O-A 0.6182 0.2428 < 0.0001 Tukey’s p-value O-M < 0.0001 0.0254 0.2974 Tukey’s p-value P-A < 0.0001 < 0.0001 < 0.0001 Tukey’s p-value P-M 0.0003 < 0.0001 < 0.0001 Tukey’s p-value M-A < 0.0001 0.0006 0.0229 Catarrhines Chlorocebus 0.54 0.04 0.53 0.04 0.81 0.05 Macaca 0.56 0.08 0.56 0.05 0.82 0.07 Papio 1.00 0.13 0.81 0.09 0.61 0.07 Hoolock 0.43 0.03 0.51 0.02 0.90 0.03 Hylobates 0.42 0.03 0.50 0.02 0.86 0.04 Symphalangus 0.43 0.03 0.59 0.03 0.77 0.06 Gorilla 0.70 0.05 0.63 0.05 0.72 0.07 Pan paniscus 0.60 0.05 0.48 0.03 0.92 0.06 Pan troglodytes 0.65 0.04 0.48 0.03 0.79 0.04 Homo 0.37 0.02 0.32 0.02 1.11 0.08 Locomotion Orthograde 0.41 0.04 0.48 0.10 0.91 0.14 Pronograde 0.63 0.12 0.57 0.09 0.80 0.10 T-test p-value < 0.0001 < 0.0001 < 0.0001 T-test T -19.04 -6.89 -6.30 Degrees of freedom 151.75 176.42 154.31
SOM Table 7. Means and standard deviations for the angles and measurements calculated for marsupials. All angles are provided in degrees. All measurements are provided as proportions to NOC, except SBB, which is provided as a proportion to BSB, and PBR, which is provided as a proportion of PPP. SBO SD PBO SD NBO SD NAP SD PPP SD Lasiorhinus 127.81 4.83 136.22 4.76 104.51 3.87 0.70 0.04 0.98 0.05 Vombatus 117.21 6.37 127.88 6.60 95.97 5.46 0.79 0.05 0.99 0.04 Phascolarctos 115.28 10.26 129.80 9.65 98.95 8.88 0.57 0.04 0.74 0.04 Bettongia 123.66 4.47 133.77 4.15 108.46 3.90 0.64 0.03 0.84 0.04 Potorous 126.61 4.52 136.94 5.10 116.00 4.93 0.70 0.05 0.93 0.04 Dendrolagus 121.55 4.61 128.11 5.62 105.56 5.73 0.63 0.07 0.79 0.05 Macropus 122.87 8.74 128.95 9.82 96.97 7.49 0.88 0.08 1.05 0.08 Thylogale 124.29 4.99 126.75 5.70 105.39 5.91 0.68 0.04 0.87 0.04 Locomotion Bipedal 123.21 7.67 129.48 8.75 100.24 8.26 0.80 0.13 0.99 0.12 Orthograde 115.28 10.26 129.80 9.65 98.96 8.88 0.57 0.04 0.74 0.04 Quadrupedal 122.42 6.33 131.28 7.03 106.06 9.11 0.70 0.09 0.90 0.10 Tukey’s p-value B-O < 0.0001 0.3568 0.0025 < 0.0001 < 0.0001 Tukey’s p-value B-Q 0.0003 0.7253 0.0002 < 0.0001 < 0.0001 Tukey’s p-value O-Q 0.7916 0.9852 0.8227 < 0.0001 < 0.0001 PBR SD BOS SD BSB SD SBB SD Lasiorhinus 0.36 0.01 0.48 0.02 0.23 0.01 0.50 0.13 Vombatus 0.35 0.02 0.49 0.03 0.23 0.02 0.44 0.09 Phascolarctos 0.52 0.03 0.47 0.03 0.20 0.01 0.50 0.07 Bettongia 0.40 0.03 0.42 0.05 0.17 0.03 0.44 0.13 Potorous 0.35 0.02 0.38 0.02 0.15 0.01 0.73 0.11 Dendrolagus 0.51 0.02 0.46 0.03 0.20 0.02 0.52 0.07 Macropus 0.45 0.03 0.46 0.02 0.20 0.02 0.57 0.11 Thylogale 0.46 0.02 0.46 0.02 0.18 0.01 0.53 0.06 Locomotion Bipedal 0.44 0.03 0.45 0.03 0.19 0.02 0.54 0.12 Orthograde 0.52 0.03 0.47 0.03 0.20 0.02 0.50 0.07 Quadrupedal 0.41 0.08 0.44 0.05 0.20 0.04 0.56 0.15 Tukey’s p-value B-O < 0.0001 0.3941 0.1767 0.3826 Tukey’s p-value B-Q 0.0016 0.3302 0.3837 0.6185 Tukey’s p-value O-Q < 0.0001 0.0573 0.6111 0.1180