THE ANATOMICAL RECORD 298:180–194 (2015)

Geometric Morphometrics of Hominoid Infraspinous Fossa Shape DAVID J. GREEN,1* JESSE D. SERRINS,1,2 BRIELLE SEITELMAN,1 AMY R. MARTINY,1,3 AND PHILIPP GUNZ4 1 Department of Anatomy, Midwestern University, Downers Grove, Illinois 2 Rowan University School of Osteopathic Medicine, 42 East Laurel Road, Stratford, NJ 08084 3 Anatomical Gift Association of Illinois, 1540 South Ashland Avenue, Chicago, IL 60608 4 Department of Human Evolution, Max Planck Institute, Deutscher Platz 6, 04103 Leipzig, Germany

ABSTRACT Recent discoveries of early hominin scapulae from Ethiopia (Dikika, Woranso-Mille) and South Africa (Malapa) have motivated new examinations of the relationship between scapular morphology and locomotor function. In particular, infraspinous fossa shape has been shown to significantly differ among hominoids. However, this region presents relatively few homologous landmarks, such that traditional distance and angle-based methods may oversimplify this three-dimensional structure. To more thoroughly assess infraspinous fossa shape variation as it relates to function among adult hominoid representatives, we considered two geometric morphometric (GM) approaches—one employing five homologous landmarks (“wireframe”) and another with 83 sliding semilandmarks along the border of the infraspinous fossa. We identified several differences in infraspinous fossa shape with traditional approaches, particularly in superoinferior fossa breadth and scapular spine orientation. The wireframe analysis reliably captured the range of shape variation in the sample, which reflects the relatively straightforward geometry of the infraspinous fossa. Building on the traditional approach, the GM results highlighted how the orientation of the medial portion of the infraspinous fossa differed relative to both the axillary border and spine. These features distinguished Pan from Gorilla in a way that traditional analyses had not been able to discern. Relative to the wireframe method, the semilandmark approach further distinguished Pongo from Homo, highlighting aspects of infraspinous fossa morphology that may be associated with climbing behaviors in hominoid taxa. These results highlight the ways that GM methods can enhance our ability to evaluate complex aspects of shape for refining and testing hypotheses about functional morphology. Anat Rec, 298:180–194, C 2014 Wiley Periodicals, Inc. 2015. V

Key words: scapula; infraspinous fossa; geometric morphometrics; three-dimensional; hominoid

Grant sponsors: Midwestern University Dr. Kenneth A. Suarez Fellowship, Wenner-Gren Foundation: National Science Foundation IGERT Grant (9987590); NSF Doctoral Dissertation Improvement Grant (BCS-0824552). *Correspondence to: David J. Green, Ph.D.; Department of Anatomy, Midwestern University, 555 31st Street, Downers Grove, IL 60515. Fax: 630-515-7199. E-mail: [email protected] C 2014 WILEY PERIODICALS, INC. V

Received 3 October 2014; Accepted 11 October 2014. DOI 10.1002/ar.23071 Published online in Wiley Online Library (wileyonlinelibrary. com).

THREE-DIMENSIONAL INFRASPINOUS FOSSA SHAPE

INTRODUCTION Scapular morphology has long been used to draw anatomical links with the locomotor activities of extant organisms for the purpose of reconstructing the paleobiology of extinct forms, particularly hominins (Inman et al., 1944; Ashton and Oxnard, 1964; Oxnard, 1967; Roberts, 1974; Stern and Susman, 1983; Susman et al., 1984; Susman and Stern, 1991; Larson, 1995; Young, 2008). Unfortunately, primate scapulae are not readily preserved in the fossil record, and when recovered, are usually limited to fragments of the glenoid and adjoining borders (Vrba, 1979; Johanson et al., 1982; Berger, 1994; Toussaint et al., 2003; Lordkipanidze et al., 2007). Since the discovery of the Dikika (Ethiopia) baby (Alemseged et al., 2006), however, several additional early hominin scapulae from Woranso-Mille, Ethiopia (Haile-Selassie et al., 2010) and Malapa, South Africa (Berger et al., 2010; Churchill et al., 2013) have come to light, each nearly complete or preserving considerable portions of the scapular blade. These discoveries have, in part, contributed to a renewed interest in comparative scapular anatomy (Young, 2008; Green and Alemseged, 2012; Bello-Hellegouarch et al., 2013b; Green, 2013) and shoulder functional morphology (Potau et al., 2011; Larson and Stern, 2013; Roach et al., 2013). Two recent investigations of extant hominoid and fossil hominin scapular remains highlighted several scapular features that distinguish taxa by locomotor behavior (Green and Alemseged, 2012; Green, 2013). These studies also identified portions of the scapular blade that appear to change throughout ontogeny in response to modifications in locomotor activity. These results highlighted the utility of scapular morphology for making interpretations about function, and in particular, identified several dorsal scapular fossa traits that (1) successfully sorted extant groups and (2) appeared to be particularly susceptible to in vivo changes in response to locomotor shifts. Building on these findings, this study focuses on the shape of the infraspinous region for two major reasons: (1) its shape has been found to successfully separate hominoid taxa by broad locomotor categories (Roberts, 1974; Larson, 1995; Young, 2002; Green, 2010) and (2) Larson and Stern (1986) found that the infraspinatus muscle (of which the infraspinous fossa serves as its origin site) was the only rotator cuff muscle consistently recruited during suspensory behaviors in Pan. Accordingly, infraspinous fossa morphology ought to be particularly useful for reconstructing the locomotor behaviors of extinct hominoids. Arboreal hominoids possess superoinferiorly narrower infraspinous regions relative to the broader fossae displayed by modern humans (Larson, 1995; Young, 2002; Green, 2010). Recently, Green and Alemseged (2012) noted that the Australopithecus scapula possessed similarly apelike infraspinous characteristics and hypothesized that this morphology might represent a more effective configuration for infraspinatus’ role in stabilizing the shoulder joint during suspensory activities (Larson and Stern, 1986; Larson, 1995). At the same time, these studies have also identified morphological convergences that are at odds with the functional hypotheses. For example, the scapulae of Pongo and Homo share many similar traits, despite the vast differences in locomotor habits between them

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(Bello-Hellegouarch et al., 2013b; Green, 2013; Larson and Stern, 2013). One potential shortcoming of previous studies is that many of them relied on traditional morphometric methods—namely, simple ratios of linear and angular measures—to evaluate scapular shape differences. However, the nature of the scapular blade means that traditional approaches are restricted to a small number of discrete landmarks. This limits the resolution of these data, possibly clouding subtle traits that might distinguish groups. Our goal is to investigate infraspinous fossa morphology using additional methods to explore shape. Traditional studies enable one to target specific features for investigation, which makes it relatively easy to assess how individual traits vary across taxa. However, it is more difficult to appreciate how these traits covary using these approaches. For example, if trait “X” is greatly exaggerated in one group but not another, does its expression affect trait “Y” similarly in both groups, or might the manifestation of traits “X” and “Y” be expressed independently of one another? Depending on the complexity of the shape in question, traditional approaches might oversimplify the morphology. Several recent scapular studies have focused on the most appropriate and effective methods for comparing morphology in addition to assessing shape differences (e.g., Bello-Hellegouarch et al., 2013b; Larson and Stern, 2013). Most scapular landmarks can be considered Type 2 or 3 landmarks, such as the maximum/minimum of a local curve, or a directional identifier like the anteriormost point of a particular bony feature. These landmarks tend to be less repeatable and may amplify interor even intraobserver error, calling into question the homology of the landmarks and shapes under consideration. In contrast, Type 1 landmarks, which represent the convergence of discrete tissues, such as the intersection of cranial sutures, are preferable (Bookstein, 1997b; Zelditch et al., 2004). Traditional depictions of scapular shape may be adequate for identifying major differences across taxa, but to better understand specific regions, especially those lacking repeatable landmarks, it is imperative to have additional tools to capture scapular shape (BelloHellegouarch et al., 2013b; Larson and Stern, 2013). While it may be simple enough to assess differences in superoinferior infraspinous breadth near the medial and lateral aspects of the fossa using traditional landmarks, for example, it is more challenging to evaluate fossa shape between these points. Problems may also occur when gross morphological differences are qualitatively apparent, but difficult to convey quantitatively (Green, 2010). Recent studies have applied geometric morphometric (GM) methods to investigate scapular morphology (Taylor and Slice, 2005; Young, 2008; Melillo, 2011; BelloHellegouarch et al., 2013a). GM techniques represent a wide range of analytical methods aimed at evaluating shape differences, particularly in three dimensions (Rohlf and Marcus, 1993; Adams et al., 2004; Slice, 2005). GM analyses remove an object’s size and orientation in order to evaluate shape (Kendall, 1977; Zelditch et al., 2004). In this manner, GM approaches represent a step beyond traditional methods for obtaining a more comprehensive picture of the total morphological pattern. However, most GM analyses focusing on scapular morphology rely on the same discrete landmarks used to

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TABLE 1. Sample size Taxon Pan troglodytes Gorilla gorilla G.g. gorilla G.g. beringei Pongo pygmaeus Hylobates sp. H. lar H. hoolock H. agilis H. concolor H. klossii Homo sapiens

Female

Male

Unknown

Total

25 26 21 5 28 29 20 5 3 1 0 23

32 27 24 3 16 25 18 5 0 2 0 30

2 2 2 0 3 4 1 1 1 0 1 7

59 55 47 8 47 58 39 11 4 3 1 60

Data were collected from specimens housed at the National Museum of Natural History (Washington, DC), the American Museum of Natural History (New York City), the Cleveland Museum of Natural History (Ohio), the Museum of Comparative Zoology (Cambridge, MA), and the Powell Cotton Museum (Birchington, UK).

derive the traditional measures described above (Taylor and Slice, 2005; Young, 2006, 2008; Bello-Hellegouarch et al., 2013a, b). Although one can gain a better appreciation of trait interaction and covariance through GM approaches, these analyses are still limited by the availability of repeatable landmarks. One solution to this problem is to utilize semilandmarks to achieve greater coverage of a particular aspect of morphology (Bookstein, 1997a; Gunz et al., 2005; Perez et al., 2006). Semilandmarks are especially useful when the morphology in question is lacking in static, homologous landmarks—a requirement for GM analyses. Alternatively, one can compare homologous shapes by representing them as outlines or curves on which a discrete set of equally spaced semilandmarks are assigned (Gunz and Mitteroecker, 2013). The curves are resampled so that the semilandmarks are equal in number and order across the sample. In this manner, semilandmarks can be used in lieu of static landmarks to satisfy the criterion of geometric correspondence for finer-grained shape comparisons (Gunz et al., 2005). The primary goal of this study is to assess hominoid infraspinous shape variation using three different approaches: (1) traditional methods, (2) static landmark (wireframe) GM, and (3) semilandmark (curve) GM. Previous work has outlined differences among hominoids in basic infraspinous traits, such as relative breadth, length, and scapular spine orientation (e.g., Green, 2013). The goal of implementing these GM approaches is to better evaluate how these traits covary and whether or not a more comprehensive picture of morphological differences among hominoid taxa can be achieved. This speaks directly to the central question motivating this volume—do GM methods provide researchers with a more effective toolkit for assessing questions related to functional morphology? These approaches differ markedly in their labor intensity, from the time required collecting raw data to postprocessing effort in the laboratory. Although we hypothesize that the semilandmark approach will provide a more comprehensive view of the morphology, it is also the method requiring the greatest investment of time.

As such, it will be useful for future studies of the infraspinous fossa (and related structures) to determine if the semilandmark approach provides a more detailed picture that enhances evaluations of scapular functional anatomy, meriting the increased effort. Should GM provide a more detailed view of how hominoid infraspinous shape variance relates to locomotor differences than traditional approaches, it would be strong support for continued application of these methods. Alternatively, it is possible that traditional approaches are adequate for functional investigations of scapular morphology. This would be a similarly important result, indicating that future analyses can be streamlined without greatly compromising the significance of the results.

MATERIALS AND METHODS Sample Morphometric data were collected on scapulae from adult representatives (dental stages 6 and 7, following Shea, 1981; Green, 2013) of modern humans (Homo sapiens), great apes (Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus), and lesser apes (Hylobates sp.). The modern human sample was derived from both Native American and industrialized populations. The non-human sample included both mountain (G. g. beringei) and western lowland (G. g. gorilla) gorillas; most of the gibbons were Hylobates lar (Table 1).

Measurements and Analyses This study compares three different approaches to investigating infraspinous fossa shape: (1) traditional, two-dimensional measurements, (2) landmark-based GM, and (3) semilandmark-based GM. For the first two approaches, ten three-dimensional scapular landmarks were collected with an Immersion MicroScribe G2 digitizer (Fig. 1, Table 2).

Traditional

infraspinous

shape

measures.

Landmark data were used to calculate scapular lengths, indices, and angles. Angles were derived in three dimensions using R code (Ihaka and Gentleman, 1996) by calculating the intersection of two lines (i.e., four points) in space by first defining a plane on the scapula with three points and then projecting two lines within it to calculate their angle of intersection. Several linear and angle measures were considered in bivariate comparisons with dependent variables scaled either by glenoid size or a related measure (e.g., the ratio of infraspinous breadth and length). Glenoid size has been previously used to scale scapular traits (e.g., Larson, 1995; Inouye and Shea, 1997), but this measure did not scale isometrically with body mass across the wide range of primate body sizes encapsulated by this study. Using mean body masses derived from Smith and Jungers (1997), glenoid size was found to scale positively allometrically with respect to body mass (x 5 1.16, r 5 0.99), indicating that glenoid size may overestimate body size for individuals with larger body masses (e.g., male great apes). However, glenoid size and body mass scaled isometrically when only great apes and humans were considered (x 5 1.00, r 5 0.94), so glenoid size appears to at least be an acceptable proxy for overall body mass among larger-bodied hominoids (see also Green, 2013).

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Fig. 1. (a) Scapular landmarks used in this study, see Table 2 for full list, (b) axillary/medial border (AMB) angle, (c) axillary/infraspinous medial border (AIM) angle, (d) axillary border/spine (ABS) angle, (e) wireframe, and (f) semilandmark representations of infraspinous fossa shape. Images ’a-d’ modified from Schuenke et al. (2007). See Table 3 for a full list of features considered.

The significance of differences between taxa was assessed using a one-way ANOVA; the results of posthoc Tukey honest significant difference tests are reported below, given multiple comparisons. A principal components analysis (PCA) of seven linear and angular scapular measures was also performed to assess gross multivariate scapular shape differences (Table 3). PCA offers a way to visualize multivariate shape differences by generating principal component

scores, which represent the interplay of the seven characters under consideration as broad-scale shape changes (Zelditch et al., 2004). A discriminant function analysis (DFA) was also performed to test the probability that a given individual was (or was not) properly assigned to their a priori group (PCA does not assume group affiliation, while DFA does so for the purpose of significance testing). All linear values were size-corrected by glenoid size to evaluate shape differences along the first two PC

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axes; all statistical analyses described above were performed in STATISTICA (StatSoft Inc., 2011).

Geometric morphometrics of infraspinous shape. GM represent a range of analytical methods aimed at removing the effects of size and orientation to evaluate shape differences (Bookstein, 1997b; Zelditch et al., 2004; Slice, 2005). GM is particularly useful for comparing scapulae from either the right or left side and with landmarks collected using independently calibrated coordinate systems (so long as dimensions are held constant). Furthermore, this sample includes groups ranging from gibbons, which weigh only 10–11 kg, to male gorillas that can be larger than 170 kg; not correcting for size would make it the most influential factor contributing to the interspecific variance. Procrustes superimposition and thin plate spline (TPS) interpolation methods are among the most commonly applied GM methods (Zelditch et al., 2004; Gunz et al., 2012). These methods first scale objects to the same centroid size, TABLE 2. Scapular landmarks 1. Superior angle – the superior-most point of the scapula with the superior and inferior angles (point 3, below) aligned vertically with an imaginary vertebral column 2. Point of spine that meets vertebral border – a straight line from the spinoglenoid notch to the medial edge of the spine was used to select this point if the spine diminished before intersecting with the vertebral border 3. Inferior angle – the inferior-most point of the scapula with the superior and inferior angles aligned vertically with an imaginary vertebral column 4. Infraglenoid tubercle – inferomedial to point 6 (below), the origin site of the triceps brachii muscle 5. Spinoglenoid notch – the point where the base of the spine meets the blade inferior to the junction of the spine and the acromion 6. Inferior-most point of glenoid 7. Coracoid side of maximum glenoid width – anterior-most point of fossa 8. Acromion side of maximum glenoid width – posterior-most point of fossa 9. Superior-most point of glenoid 10. Point of spine above spinoglenoid notch – the union of the spine and the acromion See also Figure 1a.

after which they are rotated and translated into a common position (Fig. 2). TPS surface warps provide a way to visualize shape differences between one individual (target shape) and another or the “mean” shape. These warps can also be used to “exaggerate” shape changes to interpret how target shapes differ from the mean. This same process is utilized to interpolate semilandmarks along curves when homologous landmarks cannot be identified or in the case of missing data (see below; Gunz et al., 2005, 2012; Gunz and Mitteroecker, 2013).

Landmark-based GM of infraspinous shape. The five landmarks that best capture the boundaries of the infraspinous fossa (points 2–5 and 10; Table 2) were used to perform a simple analysis of fossa shape, hereafter known as the “wireframe” approach. GM analyses of the landmark data were performed in Morphologika (O’Higgins and Jones, 2006).

Semilandmark-based geometric morphometrics of infraspinous shape. As evinced above, only five landmarks can be reliably located to describe infraspinous shape, leaving a great deal of missing data with regard to fossa shape (Fig. 1e). Furthermore, some of the landmarks being utilized in the wireframe analysis are what Bookstein (1997b) would classify as Type 2 or 3 landmarks (e.g., point 3, which is the minimum point of a curve, the inferior angle), forcing one to relax the standards of biological and functional “homology” (Zelditch et al., 2004). To overcome these limitations, an additional approach was used to capture infraspinous fossa shape. Using the “AutoPlot” setting of the MicroScribe, the digitizer stylus was used to manually trace the border of the fossa, recording data at 1mm intervals. After removing overlapping points, using both STATISTICA (StatSoft Inc., 2011) and Morpheus (m_vis visualizer; Slice, 2007) software, this method of data capture produced threedimensional, closed curves representing the border of the origin of the infraspinous fossa (Fig. 1f). Unfortunately, it was not possible to match the static landmarks (Table 2) with the coordinates from AutoPlotcaptured points, as switching between the two settings required unique coordinate systems (though the dimensions remained the same). However, GM analyses utilizing semilandmarks distributed across a curve are more easily aligned during superimposition and preserve better

TABLE 3. List of measurements used in this study Measurement name Glenoid size Axillary/medial border (AMB) angle Axillary/infraspinous medial border (AIM) angle Axillary border/spine (ABS) angle Infraspinous breadth Infraspinous length (a) Infraspinous length (b) Infraspinous neck breadth

Description The square root of the product of glenoid height (landmarks 6–9) and width (7–8) The angle formed by the medial (between landmarks 1 and 3) and axillary (between landmarks 3 and 4) borders The angle formed by the axillary border (landmarks 3–4) and infraspinous breadth line (see below) The angle formed by the axillary border (landmarks 3–4) and the base of the spine (landmarks 2–5) The distance between landmarks 2 and 3 The “diagonal” infraspinous distance between landmarks 3 and 5 The “mediolateral” infraspinous distance between landmarks 2 and 4 The distance between landmarks 4 and 5

See also Table 2 and Figure 1 for depictions of landmarks and listed measures.

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Fig. 2. Basic superimposition procedure. (a) Depicts the infraspinous curves in shape space prior to scaling, rotation, and translation. (b) Shows all curves following scaling, rotation, and translation. The left image shows infraspinous curves in dorsal view and the right image is of the curves in oblique lateral view. The thicker lines depict group mean shapes: blue lines – Homo; orange – Pongo; gray – Gorilla; red – Pan; green – Hylobates.

geometric correspondence when static landmarks are considered in conjunction (Gunz et al., 2005). The application of GM methods requires that all objects under consideration contain the same number of points in the same order and in corresponding positions. To achieve this, the original AutoPlotted datapoints were replaced with a resampled and standardized number of points placed equidistantly along each curve. Three “anchor points” were identified post hoc that correlated as closely as possible with points 2, 4, and 10 (Figs. 3a,b and 4; Table 2). These anchor points acted as static landmarks, effectively dividing the curve into segments for resampling. The length of each curve was estimated by cubic spline interpolation (for technical details see Gunz et al., 2005; Gunz and Mitteroecker, 2013); 83 semilandmarks were evenly distributed along each curve. However, the arbitrary mathematical procedure of using equally spaced semilandmarks can result in warps with localized shape differences that relate more to point placement than actual biological properties (Fig. 3c; Bookstein, 1997a; Gunz et al., 2005). To prevent this, equidistant semilandmarks were iteratively allowed to slide along the curve, so as to minimize the thin-plate spline bending energy between each specimen and the Procrustes average shape (Fig. 4). All points were allowed to slide, including the “anchor points”. During this procedure, semilandmarks actually slide along local tangents to the curve (as opposed to the curve itself), which makes the minimization of bending energy less computationally intensive. Semilandmarks are then projected back onto the curve – following each sliding step – to ensure that no semilandmarks slide “off” of it, which would create visual artifacts unrelated to actual fossa morphology. Semilandmark sliding removes the effect from the initial spacing of the semilandmark coordinates, further avoiding visualization artifacts that can occur when

analyzing equidistant points (Gunz et al. 2005; Gunz and Mitteroecker 2013). The resultant sets of semilandmarks are not only equal in number and order but also geometrically correspondent across the sample (Fig. 3d). Whereas only five points could be used to represent infraspinous shape in the wireframe analysis, now 83 semilandmarks provide more complete coverage of overall fossa shape. After sliding, the semilandmark curves are converted to shape variables using Procrustes superimposition and then analyzed using multivariate statistics. In addition to principal component analysis (PCA), a betweengroups PCA was used to evaluate differences across groups. This technique is similar to a discriminant function analysis (DFA) in identifying group affiliation a priori, but in addition to identifying the axes that best distinguish groups, successive PC axes remain orthogonal to one another, as in a traditional PCA (and in contrast to DFA). Procrustes distances between group means were used to evaluate the significance of shape differences with permutation tests (as in Gunz et al., 2012). Distances were calculated and the grouping labels were randomly reassigned 2,000 times. P-values were calculated by dividing the number of times the scrambled Procrustes distances were greater than or equal to the actual between-group distance by 2,001 (the total number of permutations plus the original – e.g., if 20 of the permutations were greater than the actual distance, the p-value would be 0.01). We used Mathematica (Wolfram Inc., 2013) and Morphologika (O’Higgins and Jones, 2006) software packages to visualize shape differences. Group means are represented by the average of the Procrustes shape coordinates and TPS interpolation was used to compare extreme shape differences along the PC axes to the mean shape. The relative position of the groups in PC space can then be associated with shape changes along one or more PC axes.

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Fig. 3. Semilandmark procedure. (a) Curves are initially made up of a discrete number of points at 1mm intervals. (b) Autoplotted datapoints are removed and three anchoring points are assigned (see text and Fig. 4 for details on anchor points). (c) 83 equidistant semilandmarks are placed along the curve and (d) they are allowed to slide so as to minimize bending energy. Image (d) highlights that the semilandmarks do not slide very far (left image is the fossa in dorsal view, right is oblique lateral).

Fig. 4. Overlapping curves with anchor points following Procrustes superimposition; shown in dorsal, oblique lateral, and full lateral views.

RESULTS Traditional Approach to Infraspinous Fossa Shape Scapular blade shape. Axillary/medial border (AMB) angle described the overall mediolateral shape of the scapular blade, while the axillary/infraspinous medial border (AIM) angle more closely reflected the

shape of the infraspinous fossa (Green, 2013). Pan, Gorilla, and Hylobates had the narrowest scapulae, as determined by AMB angle, while Pongo and Homo were broader and did not significantly differ from one another (Table 4). Pan had the most acute AIM angle, Gorilla and Hylobates were broadest, and Homo and Pongo were intermediate.

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TABLE 4. Infraspinous fossa shape characteristics; angle or ratio value (SD) Axillary/medial border (AMB) angle (˚) Pan troglodytes Gorilla gorilla Pongo pygmaeus Hylobates sp. Homo sapiens

29.6 34.3 38.5 33.4 37.6

Axillary/infraspinous medial border (AIM) angle (˚)

(2.2)a (3.3)b (3.7)c (3.5)d (3.3)c

42.9 54.6 46.1 56.4 51.3

(4.1)a (4.0)b (4.2)c (6.8)b (3.4)e

Axillary border/spine (ABS) angle (˚) 22.6 29.8 35.3 10.3 46.0

(3.7)a (4.2)b (6.1)c (4.5)d (5.3)e

Pan troglodytes Gorilla gorilla Pongo pygmaeus Hylobates sp. Homo sapiens

Infraspinous breadth/glenoid size 3.07 (0.3)a 3.05 (0.2)a 3.33 (0.3)b 2.16 (0.4)c 3.77 (0.3)d

Infraspinous length (a)/glenoid size 5.29 (0.3)a 4.70 (0.3)b 4.65 (0.3)b 5.54 (0.3)c 4.46 (0.3)d

Infraspinous length (b)/glenoid size 3.55 (0.2)a 3.71 (0.2)b 3.27 (0.2)c 4.72 (0.4)d 3.32 (0.2)c

Pan troglodytes Gorilla gorilla Pongo pygmaeus Hylobates sp. Homo sapiens

Infraspinous breadth/length (a) 0.58 (0.04)a 0.65 (0.05)b 0.72 (0.06)c 0.39 (0.08)d 0.85 (0.05)e

Infraspinous breadth/length (b) 0.87 (0.1)a 0.82 (0.08)a 1.02 (0.1)b 0.47 (0.1)c 1.14 (0.1)d

Infraspinous “neck” breadth/glenoid size 0.80 (0.07)a 0.86 (0.08)b 0.81 (0.09)a 0.98 (0.1)c 0.91 (0.08)d

Differences between taxa were assessed by one-way ANOVA. Values with different superscript letters represent taxa that were significantly different at the a  0.05 level (e.g., Pan and Pongo for AMB angle); taxa with the same superscript were not significantly different (e.g., Pongo and Homo for AMB angle).

Scapular spine orientation. In Homo, the spine was nearly perpendicular to the medial border and the angle formed by it and the axillary border (ABS) was roughly 45 , rendering the Homo infraspinous fossa similar to that of an isosceles right triangle (Figs. 1 and 5; Tables 3 and 4). The spine was more obliquely oriented in all other taxa, particularly Hylobates, with a highly acute ABS angle indicating that the spine was nearly parallel to the axillary border. Infraspinous fossa breadth and length. Homo had the superoinferiorly broadest infraspinous fossa, relative to glenoid size (Table 4). Pongo was the next broadest, with Pan and Gorilla intermediate relative to Hylobates, which had an especially oblique scapular spine and the narrowest infraspinous fossa of all the taxa considered. Homo infraspinous fossae were also shortest diagonally (from inferior angle to spinoglenoid notch [a]), followed closely by Pongo and Gorilla; Hylobates and Pan had the longest infraspinous fossae (Table 4). The more mediolateral measure of infraspinous length (b) did not differentiate the taxa as well as the other infraspinous length measure. In fact, Pongo and Homo did not significantly differ. Gorilla infraspinous fossae were relatively longer in this dimension than Pan (a reversal from the diagonal measure of length); Hylobates was longest of all the taxa considered (Table 4). With the superoinferiorly broadest and mediolaterally shortest infraspinous fossa, Homo had the greatest infraspinous breadth:length ratio of all the taxa. Pongo was the closest to Homo in both instances and Hylobates had the smallest ratio for both infraspinous breadth:length considerations (Table 4). Gorilla and Pan were intermediate in both cases; Pan and Gorilla did not significantly differ in the more transverse consideration of infraspinous length, but Gorilla fossae were broader than those of Pan, relative to the more diagonal (a) measure (Table 4).

Infraspinous fossa “neck” breadth. Hylobates and Homo had the widest infraspinous necks, followed by Gorilla and Pongo and Pan, the latter of which did not significantly differ from one another (Table 4). Multivariate scapular shape characteristics. The first two PC axes accounted for nearly 80% of the variance in the sample, with the first PC explaining a little more than half. The Hylobates data scatter was almost entirely by itself in positive PC 1 shape space, while there was a considerable amount of overlap between Pongo and Homo along the negative end of this axis (Fig. 6). The two measures of infraspinous length contributed to the positive position of Hylobates, while ABS angle and infraspinous breadth contributed most to the negative position of Homo and Pongo (Table 5). Gorilla and Pan were quite similar in their PC 1 scores, but Pan occupied more of the positive PC 2 space relative to Gorilla. Similarly, some of the Pongo scatter extended into positive PC 2 space, while Homo predominated the negative end of both axes (Fig. 6). Infraspinous length had the strongest PC load score in the positive direction for PC 2, while AIB and AMB angles had the strongest negative load score, along with infraspinous neck breadth. All taxa were significantly different in the DFA (p < 0.001); Pan and Gorilla (10.8) and Pongo and Homo (11.3) had the smallest Mahalanobis D2 distances, but the groups were still significantly different from one another.1

1

Pan individuals were correctly classified 96.8% of the time (two were misclassified as Gorilla), Gorilla individuals were correctly classified 92.7% of the time (three as Pan, one as Homo), Pongo individuals were correctly classified 89.6% of the time (two as Pan, three as Homo), Hylobates individuals were correctly classified 91.5% of the time (three as Pan, two as Gorilla) and Homo individuals were correctly classified 98.4% of the time (one as Pongo).

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Individuals that fell along the extreme positive end of PC 1 had superoinferiorly constricted infraspinous fossae that were mediolaterally elongated relative to the mean shape – a typical shape for Hylobates and some Pan individuals. Alternatively, the extreme negative PC 1 infraspinous fossa shape was superoinferiorly broader, particularly along the medial border, and relatively shorter in the mediolateral dimension. It is further apparent that the superoinferior breadth of the infraspinous fossa was broader medially relative to the lateral portion of the fossa in individuals with more negative PC 1 scores (e.g., most of Homo and some Pongo individuals). As suggested above, scapular neck breadth did not dramatically differ across the sample. Instead, individuals residing in positive PC 1 space had infraspinous fossae that were similarly broad from the scapular neck to the medial border (and possibly even narrower medially in extreme cases; Fig. 7). The second PC explained 16.5% of the variance in the sample and showcased a slight divergence in African ape infraspinous shape (Fig. 7). Most Pan individuals had relatively shorter scapular spines with a more obtuse angle between the spine and medial border. In contrast, most Gorilla spines were relatively longer and formed a more acute angle with the medial border. The principal characteristic driving separation of the taxa along PC 1—superoinferior infraspinous breadth (i.e., points 2 to 3 [infraspinous breadth]; Table 2)—did not dramatically differ in PC 2. Instead, variation along this axis was driven by the orientation of the infraspinous portion of the medial border relative to the spine (Fig. 7).

Semilandmark GM Approach to Infraspinous Fossa Shape

Fig. 5. Dorsal (left) and oblique lateral (right) depictions of typical infraspinous curves for each of the hominoid taxa considered in this study.

“Wireframe” GM Approach to Infraspinous Fossa Shape Figure 1e displays the wireframe representation of the infraspinous fossa. The first two principal component axes of the wireframe Procrustes shape scores explained more than 85% of the variance in the sample, with PC 1 accounting for nearly three-quarters of it. As in the previous PCA, Homo and Hylobates fell on the extreme low and high ends of PC 1, respectively, while the African apes and Pongo had similar PC 1 scores (Fig. 7).

Figures 1f and 5 depict the semilandmark/curve representation of the infraspinous fossa. As in the wireframe analysis, the first two principal component axes of the semilandmark PCA explained just less than 90% of the variance in the sample, but PC 1 accounted for nearly 80% of the total sample variance (Fig. 8). The semilandmark results largely agreed with those from the wireframe analysis regarding the principal shape differences along the first two factor axes. Superoinferior infraspinous breadth was the major factor separating the taxa along PC 1, and the uniformly constricted shape of the Hylobates infraspinous was contrasted with that of Homo and a few Pongo individuals (Fig. 8). The relative spine/medial border length differences identified above in PC 2 were also noticeable in this analysis, but the separation between Gorilla and Pan was not as marked. Intraspecific variance was greatest in Pongo and Hylobates, with individuals from these groups occupying a much wider range of shape space than Homo and the African apes (Fig. 8). Most Hylobates occupied the extreme positive PC 1 and negative PC 2 space, however, there were a number of individuals whose infraspinous fossae were closer to the mean shape and more similar to Pan. Likewise, most Pongo individuals possessed infraspinous fossae that were intermediate between Gorilla and Homo, but several individuals additionally possessed broader infraspinous regions (i.e., negative PC 1 scores) with relatively short scapular spines (positive PC 2). This configuration distinguished several Pongo individuals from Homo along PC 2 and

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Fig. 6. PCA of seven traditional measures. See also Tables 3–5.

represented a unique shape among the taxa that was not as evident from the wireframe analysis (Fig. 8).

DISCUSSION This study compared the results of three different approaches to evaluating infraspinous fossa morphology among hominoids. First, we summarized the results of a traditional, two-dimensional consideration of linear and angular measures (see Green, 2013 for a more complete discussion). Next, we compared these results to those obtained from two geometric morphometric applications: one using five static infraspinous landmarks (wireframe) and another with 83 semilandmarks (curve). By and large, all three approaches identified superoinferior infraspinous breadth at the medial end of the fossa as the major factor distinguishing the groups. As highlighted elsewhere, the traditional approaches did a reasonable job of identifying the major morphological characteristics that distinguish the taxa. We were also interested in comparing how the two GM approaches performed relative to one another. Both analyses returned similar results, but the semilandmark analysis resulted in a slightly clearer separation between Pongo and Homo, particularly in the medial aspects of infraspinous shape (which also distinguished

Pan from Gorilla, while highlighting some correspondence between Pan and Hylobates; Fig. 8). For the most part, however, the static landmarks did a sufficient job of capturing important infraspinous fossa shape attributes. The infraspinous fossa has a relatively simple geometry, one that can be convincingly represented as two adjacent triangles (one as the blade, and another, the spine projecting posteriorly and superiorly from it; Fig. 7). This is not to say that a semilandmark approach is unnecessary in all cases, but it might have been somewhat redundant for a simpler shape like the infraspinous fossa. In contrast, more complex anatomical regions—for example, the supraspinous fossa—are likely to benefit from the increased resolution of a semilandmark analysis (e.g., Green et al., 2014). Although the traditional approach was useful for detecting individual characteristics (e.g., Larson, 1995; Green, 2013), the GM methods improved our ability to recognize sets of covarying characters (Taylor and Slice, 2005). Accordingly, we identified two major morphotypes that categorize the scapular shape of an arboreal hominoid. On the one hand, suspensory taxa possess infraspinous fossae that are superoinferiorly compressed throughout, with relatively long and obliquely oriented scapular spines. These scapulae characterize groups like Hylobates and Pan, which occupied positive PC 1 space

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TABLE 5. List of measurements used and the first two factor load scores in ascending order for the PCA depicted in Figure 6 Axillary border/spine angle Infraspinous breadth Axillary/medial border angle Axillary/infraspinous border angle Infraspinous neck breadth Infraspinous length (a) Infraspinous length (b)

PC 1

PC 2

20.936 20.883 20.392 0.382 0.393 0.793 0.928

20.823 20.787 20.578 20.227 20.175 0.088 0.452

Axillary/infraspinous border angle Axillary/medial border angle Infraspinous neck breadth Infraspinous length (b) Axillary border/spine angle Infraspinous breadth Infraspinous length (a)

See also Table 3 and Figure 1 for depictions of listed measures.

Fig. 7. PCA of wireframe Procrustes shape coordinates. Red, dotted wireframe images represent the mean shape; black warped images represent extreme infraspinous fossa wireframe target shapes along the respective PC axes. Both dorsal and oblique lateral views are shown.

(Figs. 7 and 8), and also Gorilla and Pongo to a lesser extent (Fig. 5). In contrast, Homo infraspinous fossae are broader at the medial end, with relatively short, transversely oriented spines. Thus, the principal shape change from Hylobates to the African apes, Pongo, and finally Homo would be that the fossa becomes progressively less trapezoidal (with one parallel side) and more like an irregular trapezium, with the medial edge becoming significantly broader than the lateral-most

portion (Fig. 5). In part, this shape is achieved as the orientation of the spine shifts from an oblique orientation in Hylobates (situated almost superiorly) to a more transverse one in Homo. Taxa with the most positive PC 1 scores were also the most arboreal: Hylobates, followed by Pan and Gorilla. Pongo breaks with this trend, although, with a more quadrumanous style of arboreal locomotion, orangutan suspensory behavior is vastly different from that of

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Fig. 8. PCA of semilandmark Procrustes shape coordinates. Red, dotted curve images represent the mean shape; black, warped images represent extreme infraspinous fossa curve target shapes along the respective PC axes. Both dorsal and oblique lateral views are shown.

gibbons and the African apes (Larson, 1995; Thorpe and Crompton, 2005, 2006; Young, 2008; Green 2013). Accordingly, it may not be surprising to find such gross morphological differences between the scapulae of Pongo and Hylobates and the African apes. However, an additional source of confusion following the traditional approach was the convergent morphological trend between Pongo and Homo (Table 4). In contrast, the GM results identified several traits that distinguished Pongo from Homo, especially along PC 2 (Figs. 7 and 8). A good number of Pongo individuals (particularly those with lower PC 1 scores) occupied the more positive regions of PC 2, along with a number of Hylobates individuals and Pan, which may represent a second “arboreal” scapular morphotype. As before, these individuals had more obliquely oriented scapular spines, but unlike the individuals that typify the positive PC 1 group, this infraspinous fossa shape was achieved with a relatively shorter spine that is roughly equal to the breadth of the infraspinous medial border (Figs. 5, 7 and 8). As such, these fossae combine an obliquely oriented scapular spine with a relatively broader infraspinous medial border and a more sharply acute inferior angle. Unlike previous traditional assessments (Table 4; Larson, 1995; Green, 2013), our GM results indicated that

Pongo infraspinous fossae display a unique combination of characteristics that distinguish them from Homo. In fact, these traits also separated Pan from Gorilla, which is consistent with behavioral data that showed Pan to be more arboreal than Gorilla (Doran, 1997). The traditional analysis showed the African apes to have similar infraspinous breadth measures, but they differed in relative spine length and orientation (see also Fig. 5; Table 4; Larson, 1995; Bello-Hellegouarch et al., 2013b; Green, 2013). Gorilla possessed longer and more transversely oriented scapular spines than Pan (i.e., a more acute angle between the spine and the infraspinous portion of the medial border; Figs. 7 and 8). This example highlights how correspondence between taxa in a single measure (e.g., infraspinous breadth) can be expressed differently, resulting in divergent overall shapes. Furthermore, the different orientation of the infraspinous medial border between Pan and Gorilla was not as clear from the traditional analysis as it was following the GM analyses. Examples like this reveal some of the limitations of traditional methods where GM analyses might prove to be a useful complement. The major differences between Homo and Hylobates drove the morphological signal, so it is not surprising that subtle aspects of African ape morphology were

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harder to separate with the traditional approach relative to the GM methods. Importantly, differences in the shape of the medial portion of the infraspinous fossa (i.e., where the spine meets the medial border) also linked Pan more closely with the highly suspensory Hylobates than the more quadrupedal Gorilla. Furthermore, Pongo diverged from Homo, much in the same way as Pan differed from Gorilla (particularly in the semilandmark analysis). As a whole, the infraspinous fossae of Pongo, Pan, and Hylobates were more obliquely oriented than most Gorilla and Homo. In this way, our GM results highlighted portions of Pongo infraspinous fossa shape that were more similar to Pan and Hylobates (Figs. 5 and 8). The combination of a relatively narrower infraspinous medial border, oblique scapular spine, acute inferior angle (AIM angle), and obtuse angle between the spine and infraspinous medial border distinguished most Pongo from Homo while uniting the former with Pan and Hylobates—the most arboreal groups in the sample. With a more obliquely oriented and superoinferiorly compressed infraspinous fossa, Hylobates presents an extreme example of a morphology that facilitates a more efficient line of action of the infraspinatus muscle (Fig. 5; Larson, 1995). Larson and Stern (1986) found this arrangement to be crucial for maintaining glenohumeral joint stability during suspensory activities while also resisting transarticular stress. Our traditional approach did not suggest that Pongo fit into this morphotype, despite their well-documented arboreal preference (Sugardjito and van Hooff, 1986; Cant, 1987; Thorpe and Crompton, 2005, 2006). However, our GM results present a different case. Although the Pongo infraspinous breadth was greater than Hylobates, this morphology is also coupled with a significantly shorter spine (Green, 2013), such that the Pongo infraspinous fossa – and that of Pan – can be further characterized as having a more obtuse union between the spine and the medial border, effectively lengthening the inferior portion of the infraspinous fossa relative to the more superior region near the spine. Larson and Stern (2013) recently reported the results of electromyography experiments with Pongo, Pan, and Hylobates that reinforced their contention about the infraspinatus muscle acting to resist transarticular stress (Larson and Stern, 1986). For Pongo, however, they found that only the lower 2/3 of the infraspinatus muscle was active during support phase of armswinging, while the superior-most portion of the muscle was silent. Larson and Stern (2013) contended that the inactivity of this portion of the muscle, which is closest to the more transversely oriented spine, reflected its suboptimal line of action about the shoulder joint. Our GM results accord with these interpretations, since the inferior portion of the Pongo infraspinous is elongated and more like the morphology seen in Pan, as well as Hylobates (Figs. 5, 7, and 8). Both Pan and Pongo share short “spinal” infraspinous regions that are relatively elongated inferiorly, which is more reminiscent of the Hylobates shape (Table 4). These details would not have been obvious from less detailed assessments of relative scapular fossa morphology (as summarized by Larson and Stern 2013). As such, the traits identified in this study represent several features that facilitate suspensory behaviors in these groups and can be thought of as characteristic of arboreal hominoid scapulae.

Our GM analyses increased the resolution of fossa shape differences among hominoid primates relative to more traditional approaches. This is not to say that traditional approaches are irrelevant, rather, we found that GM complemented and enhanced the morphological insights gleaned from traditional methodologies, and vice versa. In fact, these GM analyses helped identify additional characters that drove morphological differences among the groups. For example, it was previously noted that the African apes possessed obliquely oriented scapular spines, as determined by their acute axillary border/spine angle (Table 4; see also Larson, 1995; Young, 2008; Bello-Hellegouarch et al., 2013b; Green, 2013). Similarly, traditional methods had determined that the Gorilla medial border forms a more obtuse angle with the axillary border than Pan. However, we had not previously tested differences in the angle formed by the spine and the infraspinous portion of the medial border. Our GM analyses showed that this feature may be a principal trait that differentiates Pan from Gorilla, and also Pongo from Homo, implying that it should be an important feature for future considerations of both modern and fossil hominoid scapular morphology. Previous work associated a more compressed and obliquely oriented infraspinous fossa with suspensory behaviors in hominoids (Larson, 1995; Green, 2013), and possibly Australopithecus (Green and Alemseged, 2012). However, similarities between Homo and Pongo warranted further investigation (see also Fig. 6, Table 4; Young, 2008; Bello-Hellegouarch et al., 2013b; Larson and Stern, 2013). Through our GM analyses we were able to identify additional aspects of the infraspinous fossa that further differentiated Pongo from Homo, while also aligning the former with Pan and Hylobates. These assessments enabled us to investigate the covariance of several infraspinous fossa traits, which was more difficult to do with traditional analyses where traits are considered individually or as bivariate ratio comparisons. In this manner, GM has enhanced the resolution of infraspinous fossa variation and as a result, our ability to make functional inferences about shape differences among the hominoids.

ACKNOWLEDGEMENTS The authors sincerely thank C. Terhune and S. Cooke for inviting us to participate in this symposium and volume. They also wish to acknowledge A. Gordon for analytical assistance and D. Hunt and L. Gordon (NMNH), E. Westwig, I. Tattersall, and G. Garcia (AMNH), J. Chupasko and M. Omura (MCZ), Y. Haile-Selassie and L. Jellema (CMNH), and M. Harman and A. Gill (PCM) for coordinating museum visits.

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