Morphology of the Distal Radius in Extant Hominoids and Fossil Hominins: Implications for the Evolution of Bipedalism

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1 THE ANATOMICAL RECORD 295: (2012) Morphology of the Distal Radius in Extant Hominoids and Fossil Hominins: Implications for the Evolution of Bipedalism MELISSA TALLMAN* Department of Anthropology, City University of New York and NYCEP, New York, New York ABSTRACT One of the long-standing arguments about the evolution of bipedality centers on the locomotor pattern used by the last common ancestor (LCA) of apes and humans. In particular, knuckle-walking has been suggested as this locomotor pattern on the basis of shared morphology in the upper limb between African apes and humans and phylogenetic parsimony. Using three-dimensional geometric morphometrics, this study tests whether the distal radius of extant hominoids is sufficient for determining locomotor pattern and the affiliations of Plio-Pleistocene hominins to the extant taxa. Results indicate that while the entire radius differentiates the extant taxa very well by locomotor pattern, the distal radius fails to clearly differentiate the extant taxa. The sigmoid notch of the distal radius is the anatomical feature that differs most among the extant taxa, and its variability broadly correlates with necessary mobility at the wrist joint. Principal components and discriminant function analyses indicate that early hominins are affiliated with a variety of extant taxa with different locomotor patterns. Overall, the bony anatomy of the distal radius of early hominins points towards something adapted for a wide variety of locomotor postures. Anat Rec, 295: , VC 2012 Wiley Periodicals, Inc. Key words: geometric morphometrics; knuckle-walking; functional morphology; Plio-Pleistocene hominins INTRODUCTION Evidence from the forelimb could potentially be used to reconstruct the posture that gave rise to bipedalism. One of the ongoing arguments surrounding the evolution of bipedalism centers on the locomotor pattern that was the direct precursor to bipedalism. At different times, the last common ancestor (LCA) has been reconstructed to have quite different locomotor repertoires based on traits in the forelimb. For instance, the LCA has been reconstructed to be a hylobatid-like brachiator (Keith, 1903), based on the retention of suspensory characteristics in the shoulder joint (Tuttle, 1969). Alternatively, it has been said to be an antipronograde, vertical-climber, based on convergence in wrist morphology of lorises and suspensory hominoids (Cartmill and Milton, 1977) and observational data on orangutan locomotion in terminal branches (Crompton and Thorpe, 2007; Thorpe et al., 2007). The LCA could also be a knuckle walker, based on phylogenetic parsimony (Washburn, 1967; Begun, 2003), soft-tissue anatomy adapted for weight bearing in the modern human forearm (Kelly, 2001), and the presence of stabilizing characteristics in the modern human distal Grant sponsor: WG; Grant number: 7515; Grant sponsor: NSF DDI; Grant number: ; Grant sponsor: NSF; Grant number: ; Grant sponsor: NYCEP; Grant number: *Correspondence to: Melissa Tallman, American Museum of Natural History, Division of Vertebrate Paleontology, 79th Street at Central Park West, New York, NY ltallman@gmail.com Received 3 August 2011; Accepted 21 December DOI /ar Published online 20 January 2012 in Wiley Online Library (wileyonlinelibrary.com). VC 2012 WILEY PERIODICALS, INC.

2 DISTAL RADIUS MORPHOLOGY IN HOMINOIDS AND HOMININS 455 radius (Richmond and Strait, 2000). Or, it could be a generalized terrestrial quadruped, based on weight-bearing traits in the modern human wrist (Gebo, 1996). Selective pressures were likely strongest on the hindlimb during the shift to bipedalism while selection on the forelimb would have been lessened as the forelimbs are not involved in bipedal locomotion. Therefore, it may be possible to detect a locomotor signal from the forelimb in the earliest hominins other than that of bipedalism that would inform us on the locomotor pattern of the last common ancestor (Begun, 2003). It has been suggested that the distal radius could be an important place to look for such locomotor adaptations (Richmond and Strait, 2000; Richmond et al., 2001). Knuckle walking apes have distal radii that are considered to be adapted for stability during quadrupedal locomotion, including characteristics such as a distally projecting dorsal ridge, limiting dorsiflexion of the wrist during locomotion (Aiello and Dean, 1990) and a deep, enlarged scaphoid articular surface with smaller lunate articular surface, separated by a pronounced ridge (Cartmill, 1981). The entire distal articular surface is more rectangular in shape and forms an angle with the radial shaft of more than 90 degrees, which are said to be adaptations to withstand vertical forces and dorsal shearing stresses during locomotion (Jenkins and Fleagle, 1975). In contrast, Pongo and Hylobates are adapted for mobility in the distal radius. The ulnar articular surface in the distal radius is said to be modified in Pongo to reposition the joint to be orthogonal to the biomechanical forces generated during adduction of the hand in quadrumanous climbing (Sarmiento, 1985). Pongo also possesses an enlarged lunate facet and both Pongo and Hylobates have a distal radial articular surface that is less elongate than those of Pan and Gorilla. These traits are associated with a more flexible radiocarpal joint (Jenkins and Fleagle, 1975; Morbeck and Zihlman, 1988). The entire distal radial surface is more concave in Hylobates and Pongo allowing for maximal rotational ability (Jenkins and Fleagle, 1975). Until recently, there were only four Plio-Pleistocene distal radii in the African fossil record representing four different taxa: Australopithecus anamensis ( 20419), Australopithecus afarensis (A.L qv), Australopithecus africanus (Stw 46), and Paranthropus robustus (Skx 3602). Analyses using some or all of these specimens have yielded different conclusions. Heinrich et al. (1993) suggest that very early hominins had a flexible wrist adapted for quadrumanous climbing, while Richmond and Strait (2000) and Richmond et al. (2001) suggest that very early hominins had a stable wrist that retained adaptations for knuckle walking. Corruccini (1978) and Corruccini et al. (2001) similarly suggest that most early hominins, retained knuckle walking adaptations in the distal radius, but with the exception of ER Such diverse functional interpretations of the same anatomical region suggest that a reanalysis of the hominin distal radius is needed. Most previous studies have concentrated on the distal articular surface of the radius and did not incorporate information from the sigmoid notch (but see Corruccini, 1978) and all previous studies have relied on linear measurements, angles and indices. This study seeks to: 1. Test whether the distal radius is a good indicator of knuckle walking behaviors using three-dimensional geometric morphometrics (3D-GM) to quantify the shape of the distal radius. This study includes both the distal articular surface and the sigmoid notch, as well as uses information from the proximal radius and radial tubosity to assess the orientation of the distal radius in anatomical position with respect to the diaphysis and its relative size. If there is a strong knuckle walking signal from the distal radius, Pan and Gorilla should have a similar morphological signal, and that signal should be significantly different from that of the suspensory taxa and modern humans. 2. Test overall shape similarity of the fossil hominins to the extant taxa. If humans evolved from a knuckle walking ancestor, the earliest hominins (A. anamensis, A. afarensis) should be more similar to a chimpanzee/ gorilla morphotype than a suspensory morphotype. MATERIAL AND METHODS Three-dimensional geometric morphometrics (3D-GM) is a morphometric approach that allows for the retention of shape information. The shape information is preserved in most statistical analyses which allows for the visualization of shape changes among the original specimens (Rohlf and Slice, 1990). In 3D-GM, homologous points (landmarks) are selected on each specimen and data are collected as a series of x, y, z coordinates (Bookstein, 1991). Data were collected using a Microscribe 3DX digitizer; seven landmarks on the proximal radius and nine landmarks on the distal radius were recorded (Table 1; Fig. 1). The distal landmarks were designed to capture the morphology of the articular surfaces, including the scaphoid and lunate facet margins, the styloid process, and the shape and relative orientation of the sigmoid notch. Data were collected on a modern comparative sample of Homo, Gorilla, Pan, Pongo, and Hylobates, as well as original fossils (Table 2). All modern individuals were adults displaying full epiphyseal closure and non-human primates were wild shot. The modern humans were collected from a wide range of populations in order to encompass a large range of modern human variation. No casts were used in these analyses. All specimens were stabilized with modeling clay in a position such that all landmark points were able to be recorded in a single view. Where possible, the left side of each element was digitized in order to minimize random differences due to slight bilateral asymmetry. Data on all fossil specimens were collected three times and the average coordinate points were used in analyses to minimize the effects of random error. Specimens were registered with respect to one another using a Generalized Procrustes Analysis (GPA) in morphologika 2 (O Higgins and Jones, 2006). A GPA minimizes the sums of squared distances between the landmark configurations of each specimen by centering all landmark configurations on a common origin (the centroid), rotating them about this point, and adjusting them for size (Rohlf and Slice, 1990). Changes in shape from one individual to another were visualized as deformations from a reference to a target specimen (Bookstein, 1991; Adams et al., 2004). In order to examine shape differences among the extant taxa for a baseline comparison with the fossils,

3 456 TALLMAN TABLE 1. Description of landmarks taken on the radius Number Type Description Radial head 1 II Deepest point on the radial head 2 II Most medial point on radial head 3 II Most lateral point on the radial head 4 II Most anterior point on the radial head 5 II Most posterior point on the radial head Radial tuberosity 6 II Center of radial tuberosity 7 II Most distal point of the tuberosity Styloid process 8 II Tip of the styloid process Sigmoid notch 9 II Most proximoanterior point on the margin of the sigmoid notch 10 II Most proximoposterior point on the margin of the sigmoid notch 11 II Most anterior point on the facet margin of the sigmoid notch 12 II Most posterior point on the facet margin of the sigmoid notch 13 II Deepest point inside the sigmoid notch Facet margin 14 II Facet margin between lunate and scaphoid articular surfaces - most anterior point 15 II Facet margin between lunate and scaphoid articular surfaces - most posterior point 16 III Facet margin between lunate and scaphoid articular surfaces - deepest point along that line Fig. 1. Diagram illustrating the landmarks on the proximal and distal radius. principal components analyses (PCAs) were conducted on both the entire radius and just the landmarks comprising the distal radius using PAST (Hammer et al., 2001). A GPA of an entire long bone tends to emphasize length, comparative joint size and orientation of the proximal and distal ends with respect to each other over the details of shape in either epiphysis due to the way that the landmark configurations are scaled during a GPA. Shape changes in the entire radius and just the distal radius were visualized using morphologika 2 (O Higgins and Jones, 2006). A further PCA was conducted on a data set comprised of the means for each extant taxon with the fossils. Using the means of the extant taxa has the effect of weighting the fossil taxa equally to the extant taxa, thereby creating a balanced morphospace. A minimum spanning tree (MST) based on Procrustes distances was placed over the PCA in order to see which fossils and taxon means were most similar in multidimensional space. A discriminant function analysis (DFA) using SPSS v17 (SPSS, Chicago IL) was also conducted on the entire data set in order to identify the differences between known groups and to classify the fossils. In this analysis, each extant genus was given its own group and the fossils were left unclassified. Shape changes along the major axes were calculated by multiplying the eigenvectors by the maximum and minimum of each axis and adding it to the consensus configuration (Polly, 2008) and were then visualized in Morpheus (Slice, 1998). Finally, in order to assess whether the degree of variability among the fossils exceeds that of any extant species, Procrustes distances between each pair of fossils were compared with the distribution of pairwise Procrustes distances within each species and genus, as well as the pairwise distances between individuals of belonging to different genera. From these distributions, the percentage of pairs within each group with a smaller Procrustes distance than seen in each fossil pair was determined. The pairwise Procrustes distances between the fossils pairs were also compared with the pairwise distances between the extant taxon means to assess the magnitude of difference among the fossils. A similar method of assessing fossil similarity in the postcranium was used by Harmon (2009) for the proximal femur. It should be noted that while a distribution of Procrustes distances (and other distance measures like it) can provide an idea about the degree of variability within a

4 DISTAL RADIUS MORPHOLOGY IN HOMINOIDS AND HOMININS 457 TABLE 2. List of specimens used for this study by species, subspecies, and sex Males Females Unknown Total Gorilla (N ¼ 77) Gorilla gorilla beringei a Gorilla gorilla gorilla b Gorilla gorilla graueri c Homo sapiens (N ¼ 76) Andaman Islanders Australian Aborigines Late Stone Age South Africans Point Hope Ipiutak Pan (N ¼ 88) Pan paniscus c Pan troglodytes schweinfurthii c Pan troglodytes troglodytes b Pongo (N ¼ 16) Pongo pygmaeus d Hylobates (N ¼ 8) Hylobates hoolock e Fossil hominins (N ¼ 4) Australopithecus anamensis ( 20419) Australopithecus afarensis (A.L qv) Australopithecus africanus (Stw 49) Paranthropus robustus (Skx 3602) a Virunga isolates; RMCA. b Cameroon (and some gorilla males from Republic of Congo); PCM. c DRC; RMCA, AMNH-M. d Borneo, Sumatra; AMNH-M, NHM-M. e India, Myanmar; AMNH-M. given sample, it says nothing about the directionality of differences among individuals in multidimensional space in terms of shape (Bookstein, 1991). RESULTS Plots of the PCAs of the full radius and just the distal radius are presented in Fig. 2. When the entire radius is used in the analysis, there is some separation between the extant species. PC 1 separates Gorilla at one extreme and Hylobates at the other, while PC 2 separates Homo at one extreme and Pongo and Hylobates at the other. PC 1 is driven mostly by the position of the radial tuberosity on the radial shaft, as well as the size of the proximal and distal epiphyses in comparison with the full length of the bone (seen as the distance between the two epiphyses). Pongo and particularly Hylobates have small epiphyses in comparison with the length of the radial shafts, whereas Gorilla has large epiphyses and Pan and Homo are intermediate in size. Additionally, Hylobates and Pongo have radial tuberosities that are relatively close to the radial head, whereas Gorilla has the most distally located radial tuberosity. PC 1 does not have a significant relationship with centroid size (the standard test for allometric effects in 3D-GM; Bookstein, 1989). This is because PC 1 sorts the taxa based on joint size, which does not correlate with centroid size in this sample (e.g., Gorilla and Pongo have similar centroid sizes, but Gorilla has proportionally larger epiphyses than Pongo). PC 2 is driven by the angulation of the distal articular surface with respect to the long axis of the bone. Hylobates has the steepest angle between the distal articular surface and the axis of the radius, whereas in Homo the angle is close to 90 degrees. PC 2 also has no significant relationship with centroid size. Figure 2B illustrates the wireframe transformations between the means of each taxon. When the data on the proximal radius are removed, all of the information about the angle of the distal articular surface and the long axis of the bone is lost because there is no point of reference in the proximal region. This is especially relevant when considering fossils because if they are broken close to the distal articular surface, it can be difficult to determine their exact anatomical orientation. Figure 2C illustrates the results of a PCA using just the landmarks on the distal articular surface and sigmoid notch. PC 1 is driven by the width of the proximal border of the sigmoid notch, as well as the overall size of that articulation in comparison with the distal surface. Individuals with negative values on PC1 have wide proximal borders and short notches whereas individuals with positive values have narrow proximal borders and long notches. PC1 is not correlated with centroid size, and does not divide the sample in any meaningful way. PC 2 differentiates modern humans from all nonhuman extant apes and is mainly driven by the distal extension of the dorsal and palmar borders of the distal articular surface and the orientation of the sigmoid notch. In modern humans, the palmar and dorsal borders of the distal facet are practically even whereas in the nonhuman extant apes, the dorsal border (or ridge ) tends to project more distally. The sigmoid notch is also rotated more anteriorly in the nonhumans. Wireframes illustrating these differences are presented in Fig. 2D. Both of these analyses were also computed with Homo sapiens removed, but that did not improve separation between the nonhuman extant apes and thus the results are not shown. The results of a PCA and MST utilizing the taxon means and the fossils are presented in Fig. 3. PC 1 separates Stw 46 (A. africanus) at one extreme from KNM-

5 458 TALLMAN Fig. 2. A: PCA of the full radius; PC 1 accounts for 43% of the variation in this sample and PC2 accounts for 13%. B: Wireframe transformations between all taxa present in the full radius analysis. C: PCA of just the distal radius; PC 1 accounts for 21% of the variation in the sample and PC 2 accounts for 15%. D: Wireframe transformations between all taxa present in the distal radius analysis. Wireframes are ER (A. anamensis) and Gorilla at the other while PC 2 separates A.L qv (A. afarensis) at one extreme and Homo and Pongo at the other. PC 1 is driven by the distal extension of the palmar border; in Homo is it equal to the distal extension of the dorsal border whereas in Gorilla the dorsal border of the distal facet (the dorsal ridge) extends beyond the palmar border. PC 2 is driven by the angle and height of the sigmoid notch with A.L qv having a sigmoid notch oriented in a dorsal view and were taken from the center of the distribution of each taxon. An example wireframe on a Pan radius is given for comparison. In both A and C, Gorilla is represented by red crosses, Pan by pink squares, Homo by blue open squares, Pongo by green Xes and Hylobates by yellow dashes. that is most anteriorly turned and short. The MST shows that and Skx 3602 (Paranthropus robustus) share a near-neighbor relationship with Pan, despite having aspects of their shape that link them more closely with Gorilla and Homo respectively. The nearest neighbor of A.L qv is Hylobates in both 2D and multidimensional space. Stw 46 is most similar to Homo in multidimensional space, although its short sigmoid notch places it further away in the PCA.

6 DISTAL RADIUS MORPHOLOGY IN HOMINOIDS AND HOMININS 459 Fig. 3. PCA with MST of the mean extant configurations and the fossil individuals. Wireframes are in dorsal view with the sigmoid notch to the left as seen in the boxed picture of a distal chimpanzee radius. PC1 accounts for 29% of the variation in this sample and PC2 Figure 4 illustrates the graphical results of a discriminant function analysis (DFA). Despite the a priori assignation of the groups, the DFA fails to completely separate the extant taxa. In particular, there are large areas of overlap between all of the nonhuman extant apes, which are arranged along the second axis in a grade from most terrestrial (Gorilla) to most arboreal (Hylobates). The first axis is driven by the distal projection of the radial styloid and the degree of torsion in the sigmoid notch, as well as the overall width of the distal articular surface, with humans having a less rotated notch and a less projecting styloid and all nonhuman extant apes having wider distal surfaces with a more projecting styloid and greater degree of torsion. The second axis is driven by the depth of the radial articular surface and the height of the proximal border of the sigmoid notch on the palmar aspect. Gibbons have a symmetrical proximal border of the sigmoid notch and a shallower distal articular region than gorillas. The results of the fossil classification are presented in Table is classified as Gorilla, A.L qv is classified as Hylobates, but with a low probability, Skx 3602 is classified as Pan, also with a relatively low probability, and Stw 46 is classified as Homo sapiens. Cross-validation tests resulted in an accuracy rate of 86.2% correctly classified, with mistakes most frequently occurring in the classification of Pan and Gorilla (Table 4). accounts for 23%. Numbers on the graph refer to actual Procrustes distances between fossils and extant means corresponding to the links in the MST. See Table 7 for complete data on Procrustes distances. Among the fossils, is most different from Skx 3602 and Stw 46 although there were no fossil pairs where the Procrustes distance between specimens exceeded 95% of pairwise comparisons within any single extant species (Table 5). Although, due to the high degree of overlap in the extant taxa, the variability in pairwise Procrustes distances of individuals of different genera were only slightly greater on average than those in a single species or genus so it is difficult to say what conclusions can be drawn from this information regarding the differences among fossils (Table 6). However, all of the pairwise distances between the fossils exceed the pairwise differences between the extant taxon means, with the exception of Homo and Hylobates (Table 7). DISCUSSION Functional Signal in the Distal Radius The results of this analysis indicate that it is difficult to distinguish knuckle walkers from other hominoids based on the morphology of the distal radius alone. The shape of the distal radius is largely similar across the extant hominoids, except for those of modern humans which are distinctive. The differences seen, even in the discriminant function analysis, are more indicative of a locomotor grade than a clear separation into knuckle

7 460 TALLMAN Fig. 4. DFA of the Procrustes aligned landmarks of the distal radius. Fossils are marked in black and labeled in the graph. Wireframes are shown in a dorsal view with the sigmoid notch to the left. TABLE 3. Probability of group membership as determined by the DFA. Bolded values indicate the maximum probability Gorilla Homo Hylobates Pan Pongo A. anamensis (ER 20419) A. afarensis (A.L. 288) P. robustus (Skx 3602) A. africanus (Stw 46) TABLE 4. The results of the classification and cross-validation analyses for the DFA Predicted group membership Group Gorilla Homo Hylobates Pan Pongo Total Original Count Gorilla Homo Hylobates Pan Pongo Cross-validated Count Gorilla Homo Hylobates Pan Pongo Totally, 91.6% of the original cases were correctly classified and 86.2% of cross-validated individuals were correctly classified.

8 DISTAL RADIUS MORPHOLOGY IN HOMINOIDS AND HOMININS 461 Fossil pairwise distances TABLE 5. The Procrustes distances between fossils as compared with the variability within each species, subspecies, and genus A.L qv Skx Stw 46 A.L qv-Skx 3602 G. g. gorilla G. b. graueri P. t. troglodytes P. t. schweinfurthii P. paniscus P. pygmaeus H. hoolock H. sapiens Pan subsp. Gorilla sp % 51.0% 27.2% 33.9% 32.5% 40.0% 3.6% 39.5% 25.8% 14.6% 15.7% % 75.5% 66.2% 73.5% 70.8% 81.7% 21.4% 67.4% 65.9% 41.8% 50.6% % 83.2% 80.1% 88.3% 80.8% 90.8% 32.1% 78.9% 82.3% 56.9% 66.3% % 51.0% 27.2% 33.9% 32.5% 40.0% 3.6% 39.5% 25.8% 14.6% 15.7% A.L qv-Stw % 63.2% 45.8% 51.3% 54.2% 66.7% 14.3% 57.7% 45.3% 25.8% 33.1% Skx 3602-Stw % 51.0% 27.2% 33.9% 32.5% 40.0% 3.6% 39.5% 25.8% 14.6% 15.7% Average Pan sp. The Procrustes distances between each fossil comparison is given at left. Percentages indicate the number of pairs within each group that had a smaller Procrustes distance than the fossil pair. Fossil pairwise distances A.L qv Skx Stw 46 A.L qv-Skx 3602 TABLE 6. The Procrustes distances between fossils as compared with the variability between genera Gorilla- Pan Gorilla- Homo Gorilla- Pongo Gorilla- Hylobates Pan- Homo Pan- Pongo Pan- Hylobates Homo- Pongo Homo- Hylobates Pongo- Hylobates % 4.4% 8.0% 0.5% 8.5% 10.0% 0.3% 4.7% 0.0% 1.0% % 30.9% 41.7% 9.4% 37.6% 39.0% 7.7% 25.0% 0.9% 19.8% % 51.1% 62.8% 23.5% 56.8% 58.5% 18.8% 44.6% 4.8% 42.7% % 4.4% 8.0% 0.5% 8.5% 10.0% 0.3% 4.7% 0.0% 1.0% A.L qv-Stw % 14.0% 21.9% 2.8% 21.4% 22.5% 1.7% 12.0% 0.0% 5.2% Skx 3602-Stw % 4.4% 8.0% 0.5% 8.5% 10.0% 0.3% 4.7% 0.0% 1.0% Average The Procrustes distances between each fossil comparison is given at left. Percentages indicate the number of pairs within each group that had a smaller Procrustes distance than the fossil pair.

9 462 TALLMAN TABLE 7. Pairwise Procrustes distances between fossils and extant taxon means Skx 3602 Stw 46 A.L qv Gorilla Homo Pongo Pan Hylobates Skx Stw A.L qv Gorilla Homo Pongo Pan Hylobates 0 walking and suspensory locomotor patterns. In fact, only when the proximal radius was included was there separation among the extant groups due to differences in joint size and the angulation of the distal articular surface. The projection of the dorsal ridge of the radius seems to be present to some degree in all of the taxa with the exception of modern humans and assessing the differences in its distal projection seems to be at least somewhat reliant on placing the full radius in perfect anatomical position (see Fig. 2B vs. 2D). If anything, the shape and orientation of the sigmoid notch was more useful in differentiating the fossils and the extant taxa in all analyses utilizing just the distal radius. The size, shape, and orientation of the sigmoid notch are likely related to the degree of rotational ability in the wrist joint (Palmer and Werner, 1984). Evidence for a Knuckle Walking Last Common Ancestor Evidence from the distal radius has been used to argue that humans evolved from a knuckle walking ancestor (Richmond and Strait, 2000; Richmond et al., 2001). The data presented here on the distal radius lend very weak support in that direction. To rule out any kind of suspensory, Pongo-like ancestor, the plotted distribution of Pongo and the knuckle walking African apes should be separate and the oldest fossils should clearly be affiliated with the African apes. While the oldest fossil ( 20419) does fall within the African ape distribution, Pongo and Hylobates are not sufficiently different to rule that this indicates a specifically knuckle walking ancestry. Additionally, the variability among the fossil sample is consistent with both the variability within a single species (Table 5) and the variability between most of the modern pairs of genera (Table 6) due to the overlap in the shape of the extant taxa (Australopithecus anamensis; Heinrich et al., 1993) has the most ape-like distal radius. In every analysis, it falls closest to either Pan or Gorilla (Figs. 3 and 4) and the Procrustes distance between this individual and the Pan and Gorilla means is smaller than the distance between it and any of the other fossils (Table 7). The sigmoid notch of is rotated more posteriorly in comparison with Skx 3602 and Stw 46. The distal articulation is flatter and narrower than all of the other fossils in this sample and is also more flexed than Stw 46 and Skx The lunate facet is larger in comparison with the scaphoid facet, whereas the other fossils have lunate and scaphoid facets of approximately the same size. Richmond et al. (2001) associated a flexed distal articulation with knuckle walking in that a tilted distal articulation would help to close-pack the carpals and increase stability but Heinrich et al. (1993) noted the large lunate facet present and suggested that this individual might have been a good quadrumanous climber, like Pongo. As an alternative hypothesis, the presence of both of these traits might indicate a wrist that has been adapted for a wide range of functional uses. A.L qv (Australopithecus afarensis; Johansen et al., 1978) falls within the distribution of the nonhuman extant apes, and its phenetic affinities group it most closely with Pan or Hylobates (Table 7). Among the fossils, it is similar in shape to 20419, and differs from that fossil only in that it is dorso-palmarly expanded and has a less prominent styloid process. The sigmoid notch is rotated posteriorly as in Again, functionally this seems to indicate a wrist that was capable of a wide range of functional uses, including ones that would require greater stability (Richmond et al., 2001). Skx 3602 (Paranthropus robustus; Grine and Susman, 1991) is intermediate among all of the fossils. These data support the idea that Skx 3602 is quite human-like in some aspects, as originally described by Susman (2004), although is actually closer to the Pan mean shape (Table 7). The major difference between it and the extremely Homo-like Stw 46 is a more anteriorly rotated sigmoid notch. Stw 46 (A. africanus) consistently falls within the modern human distributions in all analyses and its smallest Procrustes distance is to modern humans. A. africanus is often thought to have a more ape-like postcranium reflecting the retention of arboreal adaptations (McHenry and Berger, 1998; Haeusler, 2003) although these data disagree with that conclusion. The Stw 46 distal radius only differs from modern humans in having a shorter sigmoid notch. There are no particular adaptations present for stability and thus it can be assumed that this individual s wrist could function in the same way as seen in modern humans. More recent finds include a complete radius and distal radial epiphysis of Australopithecus sediba (Berger et al., 2010) and complete radius and distal radius from Ardipithecus ramidus (White et al., 1994; Lovejoy et al., 2009). The radius from A. sediba is described only as being relatively long in comparison to the length of the forelimb (Berger et al., 2010). The two distal radii attributed to Ardipithecus ramidus are described as having a strongly angled distal articular surface with a large styloid process, palmar expansion of the radiocarpal joints, and scaphoid/lunate facet proportions just above those of Pan, within the range of Pongo and Homo sapiens. These traits have often been associated with knucklewalking behaviors (White et al., 1994; Lovejoy et al., 2009 and supplemental materials). Lovejoy et al. (2009)

10 DISTAL RADIUS MORPHOLOGY IN HOMINOIDS AND HOMININS 463 proposed that the presence of these characteristics in the distal radius of Ardipithecus ramidus in the absence of any other characters in the wrists and hands that are typically associated with knuckle walking invalidates the use of the distal radius as an indicator for the knuckle walking locomotor pattern. The data presented here do support this conclusion. Perhaps it is not surprising that there is no clear knuckle walking signal from the distal radius given the morphological and behavioral evidence relating to the ontogeny of knuckle walking characters in the modern taxa. Dainton and Macho (1999) analyzed the development of knuckle walking in chimpanzees and gorillas and found that they knuckle-walk slightly differently; gorillas stress the ulnar side of the arm and chimps the radial side. These authors also found that the shape of the carpals on the ulnar side to be significantly different in Gorilla and Pan, and that these differences could not be accounted for by differences in locomotor pattern during ontogeny in the two taxa. Kivell and Schmitt (2009) found that the development of supposed knuckle walking characteristics in the wrist followed significantly different ontogenetic trajectories in chimpanzees and gorillas and were also found in non-knuckle walking taxa. The data presented here (and elsewhere) indicate that the distal radius alone is not a strong indicator of knuckle walking capability in the extant taxa and provides little evidence that the earliest hominins evolved from a knuckle walking ancestor. If anything, the bony anatomy of the distal radius of early hominins points towards something adapted for a wide variety of locomotor postures. Given this, it is more likely that Pan, Gorilla, Pongo, and Hylobates are all too derived for specific locomotor patterns to be good models for the locomotor mode that led to bipedality. The locomotor pattern that gave rise to human bipedalism is probably not present in any extant taxon. ACKNOWLEDGEMENTS The author is indebted to the following researchers and curators for granting access to collections under their care: Emma Mbua (KNM); Mamitu Yilma (NME); Berhard Zipfel (Wits); Alan Morris (UCT); Malcolm Harmon, Powell-Cotton Museum; Louise Humphrey, Rob Kryzynsky and Paula Jenkins (NHM-London); W. Wendelen (MRAC); and Eileen Westwig and Gisselle Garcia (AMNH). Thanks as well to Eric Delson, William Harcourt-Smith, Bill Jungers and F. James Rohlf, as well as two anonymous reviewers, for their helpful comments on the preparation of this manuscript. This is NYCEP morphometrics contribution 57. LITERATURE CITED Adams DC, Rohlf FJ, Slice DE Geometric morphometrics: ten years following the revolution. Ital J Zool 71:5 16. Aiello L, Dean C An introduction to human evolutionary anatomy. London: Academic Press. Begun DR Knuckle-walking and the original of human bipedalism. In: Meldrum DJ, Hilton CE, editors. From Biped to Strider: The emergence of modern human walking, running and resource transport. New York: Kluwer. p Berger LR, de Ruiter DJ, Churchill SE, Schmid P, Carlson KJ, Dirks PHGM, Kibii JM Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science 328: Bookstein FL Size and shape : a comment on semantics. Syst Zool 38: Bookstein FL Morphometric tools for landmark data. New York: Cambridge University Press. Cartmill M Hypothesis testing and phylogenetic reconstruction. Zeitschrift für zoologische Systematik und Evolutionsforschung 19: Cartmill M, Milton K The lorisiform wrist joint and the evolution of brachiating adaptation in the Hominoidea. Am J Phys Anthropol 47: Corruccini RS Comparative osteometrics of the hominoid wrist joint, with special reference to knuckle-walking. J Hum Evol 7: Corruccini RS, McHenry HM Knuckle-walking hominid ancestors. J Hum Evol 40: Crompton RH, Thorpe SKS Response to comment on origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 318:1066. Dainton M, Macho GA Did knuckle-walking evolve twice? J Hum Evol 36: Gebo DL Climbing, brachiation and terrestrial quadrupedalism: historical precursors of hominid bipedalism. Am J Phys Anthropol 101: Grine FE, Susman RL Radius of Paranthropus robustus from Member 1, Swartkrans Formation, South Africa. Am J Phys Anthropol 84: Haeusler M New insights into the locomotion of Australopithecus africanus. Evol Anth 11: Hammer Ø, Harper DAT, Ryan PD PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4: 9 pp. Available at: Harmon E Size and shape variation in the proximal femur of Australopithecus africanus. J Hum Evol 56: Heinrich RE, Rose MD, Leakey RE, Walker AC Hominid radius from the middle Pliocene of Lake Turkana, Kenya. Am J Phys Anthropol 92: Jenkins FA, Jr, Fleagle JG Knuckle-walking and the functional anatomy of the wrists in living apes. In: Tuttle RH, editor. Primate functional morphology and evolution. The Hague: Mouton. p Johanson DC, White TD, Coppens Y A new species of the genus Australopithecus (primates: Hominidae) from the Pliocene of eastern Africa. Kirtlandia, no. 28. Cleveland, Ohio: The Cleveland Museum of Natural History. Keith A The extent to which the posterior segments of the body have been transmuted and suppressed in the evolution of man and allied primates. J Anat Physiol 37: Kelley RE Tripedal knuckle-walking: a proposal for the evolution of human locomotion and handedness. J Theor Biol 213: Kivell TL, Schmitt D Independent evolution of knuckle walking in African apes shows that humans did not evolve from a knuckle walking ancestor. Proc Nat Acad Sci USA 106: Lovejoy CO, Simpson SW, White TD, Asfaw B, Suwa G Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326: McHenry HM, Berger LR Body proportions in Australopithecus afarensis and A. africanus and the origin of the genus Homo. J Hum Evol 35:1 22. Morbeck ME, Zihlman AL Body composition and limb proportions. In Schwartz JH, editor. Orang-Utan biology. Oxford: Oxford University Press. p Morton DJ Human origins: correlations of previous studies of primate feet and posture with other morphologic evidence. Am J Phys Anthropol 10: O Higgins P, Jones N Tools for statistical shape analysis. Hull York Medical School. Available at: site/hymsfme/resources. Palmer AK, Werner FW Biomechanics of the distal radial ulnar joint. Clin Orthopaedics Related Res 187: Polly PD Adaptive zones and the pinniped ankle: a 3D quantitative analysis of carnivoran tarsal evolution. Sargis E, Dagosto

11 464 TALLMAN M, editors. Mammalian evolutionary morphology: a tribute to Frederick S. Szalay. Springer: Dordrecht. p Prost JH Origin of bipedalism. Am J Phys Anthropol 52: Richmond BG, Begun DR, Strait DS Origin of human bipedalism: the knuckle-walking hypothesis revisited. Yrbk Phys Anthropol 44: Richmond BG, Strait DS Evidence that humans evolved from a knuckle-walking ancestor. Nature 404: Rohlf FJ, Slice DE Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39: Slice DE Morpheus et al.: software for morphometric research. Revision Department of Ecology and Evolution, State University of New York, Stony Brook, New York. Stern JT Before bipedality. Yrbk Phys Anthropol 19: Susman RL, de Ruiter D, Brain CK Recently identified postcranial remains of Paranthropus and Early Homo from Swartkrans Cave, South Africa. J Hum Evol 41: Thorpe SKS, Holder RL, Crompton RH Origin of bipedalism as an adaptation for locomotion on flexible branches. Science 316: Tuttle RH Knuckle-walking and the problem of human origins. Science 166: Washburn SE Behaviour and the Origin of Man. Proc Reg Anth Inst Great Br Ireland 1967: White T, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WoldeGabriel G Ardipithecus ramidus and the paleobiology of early hominids. Science 326:75 86.