Multivariate Analysis of Early Horninid Pelvic Bones HENRY M. McHENRY AND ROBERT S. CORRUCCINI2 1 Department o f Anthropology, University of California, Davis, California 9561 6; and Division of Physical Anthropology, Smithsonian Institution, W a s h i n g t o n , D. C. 20560
KEY W O R D S Australopithecine . Pelvis . Bipedalism . Multivariate analysis. ABSTRACT Multivariate analyses of the acetabular and iliac parts of fossil hominid and extant hominoid pelvic bones show that ( 1 ) the best preserved fossil from Swartkrans (SK 3155) is more similar to the Sterkfontein pelvis (Sts 14) than either fossil is to any extant hominoid species; ( 2 ) of the living hominoids, all of the fossils are closer to modem Homo snpiens than to the apes; and ( 3 ) the robust and gracile forms of South African australopithecines are somewhat different from one another, the gracile form falling nearer to Homo sapiens, but neither form demonstrably closer to the pongids. Although the hip joint of the gracile form of early hominid is fairly well known, little information has been available about the pelvis of the robust australopithecine. Now that a new pelvic fragment (SK 3155) has been discovered (Brain, '73; McHenry, '75), the possibility exists to assess further the relationship among the early hominids and modern Homo sapiens. Divergence of opinion exists on the relationship between different kinds of fossil early hominids. The new pelvic fragment from Swartkrans can help in the resolution of this problem. The purpose of this paper is to assess the phenetic relationship of the new Swartkrans pelvic fragment through the method of multivariate analysis. This is only one step in the full analysis of the fossil, but it is a valuable undertaking in view of the disparity of opinion on early hominid locomotion (Robinson, '72; Lovejoy et al., '73; Zihlman, '69; Day, '69; Day and Wood, '68; Oxnard, '73) and the difficulty in deriving objective interpretations of fossil postcrania due to the wide variability of extant hominoid species. In the preceding article the senior author presented a traitby-trait discussion of the new pelvic fragment in comparison with other hominoids. In this paper we attempt to synthesize this information into a "total morphological pattern" through multivariate analyses which we feel is an essential step toward AM. J. PHYS. ANTHROP.,43: 263-270.
drawing coherent, objective conchsions by treating the traits as part of a single covarying complex. The hominid fossils used have all been thoroughly described (Robinson, '72; McHenry, '72, '75; Brain et al., '74). They include the new pelvic fragment from Swartkrans (SK 3155) thought to be a member of the robust australopithecine group (Paranthropus or Australopithecus robustus) by McHenry ('72, '75). One fossil classified as Paranthropus or Australopithecus robustus is included (SK 50). Three fossil pelvic fragments of the taxon Australopithecus or Homo africanus (Sts 14, MLD 7, and MLD 25) are included. Olduvai Hominid 28 (Day, '71) is treated in a separate analysis since only a small subset of our measurements is possible on this fossil. MATERIALS AND METHODS
Variability in postcranial morphology is considerable in apes and Homo. In order to obtain some appreciation of the range of variation in the shape of hominoid Felves a comparative sample was measured. The sample is presented in table l of the preceding article (McHenry, '75). Sixteen measurements were taken as described in the previous article. Many numerical techniques exist for analyzing data such as these. Multivariate 263
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HENRY M. McHENRY AND ROBERT S. CORRUCCINI
statistical methods, such as D2 and canonical variates, have been most popular in the past in anthropology. However, it has become increasingly apparent that these have a number of drawbacks (Oxnard, ’72; OXnard and Neely, ’69; Kowalski, ’72; Blackith and Reyment, ’71). Perhaps foremost among these drawbacks is that the method is not designed to consider single isolated specimens, such as a fossil of unknown affinities, unless that specimen can be assumed to be a member of one of the reference samples of extant species. Thus discriminant function analysis cannot be used to construct natural groupings, as it assumes they are known beforehand. In addition, sample sizes should be approximately equal and each sample size should exceed the number of variables employed (Corruccini, ’74). Formal statistical requirements, such as covariance homogeneity between samples and multivariate normality of distribution, are assumed to be met. Finally, discriminant function loadings seem not always to be trustworthy for interpretation (Howells, ’73). Thus there are difficulties in applying conventional multivariate analysis to individual fossils, especially when they are fragmentary, although the approach remains valuable in problems involving large samples of relatively closely related populations (e.g., extant Homo sapiens skeletal populations, Howells, ’73). Nevertheless, we shall employ canonical variates analysis to compare its results with other methods. We shall employ a simpler, non-parametric approach to reduction and ordination of measurements. The procedure follows these steps : ( a ) First each measurement is standardized by its range to insure equal weight in each variable. ( b ) A n attempt is made to adjust for within-group allometric influences, the distortion of shape by size. It is desirable to eliminate size variability as it is expressed within highly variable or sexually dimorphic species. The procedure involves correction of non-linear tendencies shown between each measurement and the standard size reference variable (Corruccini, ’72), the average magnitude of all measurements in a specimen (Mosimann, ’70). The allometry correction coefficient is a modi-
fied logarithmic coefficient of regression: averaged within Gorilla, Pongo, and Pan. ( c ) To eliminate size effects, measurements are converted to shape variables (Corruccini, ’73). This procedure resembles taking ratios between selected pairs of measurements. The problem with ratios is interpreting their variability: is the divisor increasing or the dividend decreasing? It is preferable to convert each measurement into a ratio of a single, stable variable: the standard size reference variable (Mosimann, ’70). ( d ) The shape variables are used to find distance coefficients between each pair of taxa. This distance is the square root of the average squared difference between variables in standard deviation units, the “Pythagorean”straight-line distance between points in the 16-dimensional space defined by our 16 measurements. The overall shape similarity is thus reduced to a single measure. All subjects are used in this calculation including the fossils. ( e ) Patterns followed by the shape distances are determined through cluster analysis. We employed an agglomerative clustering procedure - two taxa sharing the smallest distance coefficient join into the first cluster, their distances being averaged to the rest of the unclustered points. Then the next closest taxon joins, or another close pair may form a new cluster. The process continues until all points belong to a single cluster. The particular technique we follow is the weighted pair-group method (Sokal and Sneath, ’63). The classification process is heirarchic and does not indicate whether a point is actually intermediate between two groups -it has to join one or the other. ( f ) Cluster analysis is supplemented by principal coordinates analysis, a technique of “scaling” the distances onto axes that may be graphed, giving a plot of relationships that preserves as accurately as possible the original distances between points. Successive coordinates represent diminishing amounts of the total variance; often the first few are sufficient to indicate all the significant factors of variability. Visual assessment of natural groupings of points as they are projected onto principal coordinates can be compared with the cluster analysis.
ANALYSIS O F EARLY HOMINID PELVES
( g ) The contribution of each original measurement to the multivariate pattern of relationships can be estimated through principal component analysis. This technique is a “dual” to principal coordinates analysis (Gower, ’ 6 6 ) , in that it produces identical results in terms of distance scaling when entering variables are standardized. Principal component analysis operates on the p x p matrix of correlations between variables rather than the n x n matrix of distances between objects, finding axes (eigenvectors) of maximum variance. The resulting principal component eigenvector loadings can be converted to factor loadings, or to correlation coefficients between each variable and the component axis. Thus variables showing high correlation with a principal axis, and making a major contribution to the multivariate variation along it, can be detected. The use of these techniques in combination allows the mapping of metric variability in a reduced number of dimensions, reducing the many original raw measurements into a few shape factors. The techniques are essentially free of constraints of statistical theory and parameters, contrasting with classic multivariate statistical analyses such as canonical analysis. A canonical analysis is performed, however, for the purpose of checking the results derived by these other methods.
265 Horn0
S l i 14
MLO 7
MLO 25
SK 50
SK 3155
bp Pang0
Gorilla Hylobaies
Fig. 1 Dendrogram depicting the results of the cluster analysis described in the text. Note the fundamental bifurcation between non-human pongids and hominids (including all of the fossil hominids). Note also that the fossils classified as Australopzthecus or Homo africanus cluster together. The two specimens from Swartkrans are further removed from Homo sapiens t h a n are the gracile australopithecines.
the primary, secondary and tertiary divisions. The first bifurcation occurs between apes and hominids, entirely consistent with oFinions based upon visual inspection of primate pelves: the human shape is quite distinctive especially in its low and broad RESULTS iliac blade. All of the fossil coxal fragments The preceding article (McHenry, ’75) cluster with the human group. The second discusses the univariate pattern of varia- division on the human side is between the tion in the measurements. It is our opinion Swartkrans fossils and the rest of the that a full understanding of the pelvic bone hominids. As figure 1 illustrates, the fossils cannot derive solely from the particulate classified as “gracile” australopithecines presentation of each trait. The analysis of (Azistralopithecus or Homo africanus) all characteristics combined into multivari- cluster very tightly. ate analyses is a necessary addition toward The pongids form three clusters in this the complete understanding of the prob- analysis: Hylobntes, Gorilla and the two lem. The correlations and meaning of each genera, Pan and Pongo. It must be rememvariable presented in table 2 will therefore be discussed in terms of the multivariate bered, of course, that only the acetabulum and ilium are being considered in this analyses to be described below. The dendrogram displayed in figure 1 analysis. The wide separation of Gorilla is represents the results from the cluster not surprising considering the very wide analysis. As is true of other attempts to ilium of this genus. A more precise view of relationships depict the results of muhivariate analyses, the dendrograrn can be deceptive: Boyce can be gleaned from the similarity coeffi(’64) and many others have discussed this cients. Again, the fossil hominids are closer point. What is interesting in figure 1 are to Homo than to any ape (except for the
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HENRY M. McHENRY AND ROBERT S. CORRUCCINI
crushed and distorted SK 50 which is about equally distant from all extant hominoids). The new Swartkrans pelvic fragment is closest to SK 50, but not far from the other fossils. Caution is advised in the interpretation of this result since several crucial variables in the analysis are missing in SK 50, MLD 7 and MLD 25. This fact may influence the results concerning the very close relationship of the two Makapansgat specimens to each other and to Sts 14. One result is quite clear from the similarity coefficients: none of the fossil hominids shows a close relationship with any extant ape. The two Makapansgat specimens are nearest to modern man, while Sts 14 is next closest. The two Swartkrans fossils are considerably more distant from modern man in shape. The results of the principal coordinates analysis are eminently interpretable in terms of function of the hip joint (figs. 2 , 3, table 1 ) . The first principal coordinate accounts for about half of the total variance. Homo and the fossil hominids are widely separated from the rest of the hominoids. There is no overlap in ranges between Homo and the pongids as shown in figure 3 and the two best preserved fossils (Sts 14 and SK 3155) are very close to the
------SK
5
Fig. 2 Stereogram of the first three principal coordinates with coordinate 1 forming the axis from left to right, coordinate 2 forming the axis from front to back, and coordinate 3 forming the vertical axis.
GORILLR GDRILLil PONGO PYGIIQEUS
PRN TROGLODYTES
-
HYLOBRTES LRR
nonn
SRPIENS
SK 3155
STS 14
-\.?'
P R I N C I P R L C O l l P O N E N l ONE
Fig. 3 Range plot of the first principal coordinate. The bars include the actual range of variation on the first coordinate. Note the total separation of Homo and the pongids. Also note that on this important axis (explaining the majority of the total variance) that the two most complete fossils are very far removed from the apes and are close to the humans.
human range. The variables with high correlations with this vector are just those traits that are distinctively human : the ilium is low in Homo sapiens as it is in the fossil hominids; the distances from the center of the acetabulum to the auricular surface of the sacrum and to the posterior superior spine are small; the width of the ilium just above the acetabulum is large; the sacral surface measured as the distance between posterior iliac spines is not high; the acetabulum is deep and large; the acetabulum forms less of an angle with the ilium; the ilium is thicker in the region of the iliac pillar; and the width of the auricular surface is large. The relative width of the ilium is not nearly as important in this differentiation as the iliac height, corroborating Schultz's ('36) observation that hominid ilia were not really relatively widened so much in evolution as they were shortened. In almost all of these distinctively human characteristics the fossil hominids are like Homo sapiens. The only differences are in the size of the acetabulum which is intermediate in early hominids, and the width of the sacral articular surface which is very small in the early hominids relative to other pelvic dimensions. In sum, in the traits that best distinguish the human and ape acetabulum and ilium, the fossil hominids are distinctively
267
ANALYSIS OF EARLY HOMINID PELVES TABLE 1
Principal component loadings converted to factor coefficients which measure the relative importance of each measurement t o each axis Measurement Percent contribution
1 Htacet Transacet Wd post acet Wd ant acet Ht ilium Wd ilium 7 Min wd ilium 8 Thick ilium 9 Thick sciatic 10 Acet-postsup 11 Acet-iliop 12 Antsup-iliop 13 Antsup-postinf 14 Postsup-postinf 15 Postinf-iliop 16 Depth acet 2 3 4 5 6
Component 1
Component 2 17.7
Component 3 14.8
- 0.81 - 0.29 - 0.28 - 0.52
- 0.23
0.26 0.76 0.82 - 0.72 0.13 0.66 0.05 - 0.48 - 0.53 0.10 - 0.05 0.15 0.29 - 0.28 - 0.36 - 0.13
56.8
1.00 - 0.64 - 0.95 -0.81 - 0.65 1.oo
0.95 - 0.30 - 0.83 0.95 - 0.74 - 0.92
human except in being intermediate in the size of the acetabulum and i n the size of the sacral articular surface. The second principal coordinate is concerned with the uniqueness of the early hominid coxal fragments. On this axis Homo sapiens projects at one extreme and the fossil hominids spread out toward the opposite extreme. The variables that are highly correlated with this vector are those that describe the uniqueness of the early hominid pelves : the iliac fossa is peculiarly wide in the fossils (antsup-iliop) and the acetabulum is small. The two Swartkrans specimens project quite high on this axis but the position of SK 50 must be viewed with caution since i t is so badly distorted especially in some of these critical dimensions that distinguish the early hominids from Homo. The gracile australopithecine specimens (Sts 14, MLD 7, MLD 25) fall exactly intermediate on coordinate 2 between Homo sapiens and the Swartkrans specimens. As the first principal coordinate is concerned with the separation of hominids from the rest of the hominoids, the third principal coordinate involves the maximum division of Gorilla and Hylobates with the rest of the hominoids (including all of the hominids) falling half way between. Traits with high correlations with this axis include the width of the ilium, exceptionally large in Gorilla relative to the other vari-
- 0.56 - 0.44
- 0.20
0.08 0.42 - 0.06 0.27 - 0.21 0.08 - 0.22 0.97 0.42 0.05 - 0.43 - 0.06
ables but very narrow in Hylobates, the thickness of the bone in the region of the sciatic notch, relatively thin in Gorilla, the width of the iliac fossa ( antsup-iliop), wide in Gorilla, width of the auricular surface (postinf-iliop), relatively narrow in Gorilla compared to Hylobates, and a number of other traits. The higher coordinates account for diminishingly small amounts of the total variance. They appear to be unimportant and also uninterpretable. Figure 4 presents the first two canonical variates. Only those fossils with the entire suite of measurements are entered by necessity (SK 3155 and sts 1 4 ) . The results are similar to those found by McHenry ('72) : the first canonical variate explains the majority of the variance and acts to separate the hominids from the other hominoids. The two fossils fall with the hominids, but interestingly, SK 3155 is closer to Homo than is Sts 14. The second canonical variate separates Hylobates from Gorilla as did the third principal coordinate. The overall results are similar to the results of the principal coordinates analysis except the uniqueness of the fossils is not shown. This is to be expected since the fossils are not entered into the calculations of the canonical space but are entered as unknowns after the space is defined. Results of principal coordinates and cluster analyses of six measurements of
HENRY M. McHENRY AND ROBERT S. CORRUCCINI
St: 14 SK q155 Homa
'
Ponga
G a p
CANONICAL VARIATE
ON€
Fig. 4 Canonical analysis of the 16 coxal measurements. Note the primary bifurcation between hominids and pongids. Canonical axis I accounts for 72% of the total discrimination and axis I1 accounts for 21.5%.
Olduvai Hominid 28 (Day, '71) show how much more similar this H o m o erectus fossil is to H o m o sapiens than it is to any of the other early hominid fossils. The coefficient of similarity between H o m o sapiens and O.H. 28 is 1.18 compared to 1.40, 1.53, and 1.57 for H. sapiensSK3155, H . sapiens-Sts 14, and H . sapiens - SK 50, respectively. The similarity coefficient between O.H. 28 and SK 3155 is large (1.52), reconfirming the conclusion reached by visual inspection that the new Swartkrans fossil should not be placed in the H o m o erectzis taxon (McHenry, '75). All of the australopithecines were more similar to each other than to either H o m o sapiens or the pongids. DISCUSSION
The results of both the principal coordinates and canonical analyses show that the early hominid ilium and acetabulum are quite unpongid-like. The second principal coordinate is especially interesting in this respect: it shows that the fossils do differ from H o m o sapiens but in a phenetic direction that is independent of or at right angles to the pongid phenetic directions. Despite the australopithecine differences, they share with m a n the whole multivariate
complex which differentiates pongids from hominids. Unlike some studies (e.g., Zihlman, '70; Lovejoy et al., '73) the results here show that the gracile and robust australopithecines are somewhat different in the shape of the iliac blade and the acetabulum. Of particular interest are the differences in the relative width and shape of the iliac blade. As Robinson ('72) has pointed out on SK 50, the robust australopithecines have a characteristically broad and anteriorly expanded iliac blade which is expressed to a lesser extent in the gracile forms (Sts 14, MLD 7 and 25). Caution is required in the interpretation of SK 3155, of course. since the anterior suDerior iliac spine had to be reconstructed.- Its reconstruction was done very conservatively, however, using Sts 14 as a model (where the spine is not so beaked) as well as SK 50. The results of the canonical analysis here are similar to one of those done by Zuckerman, Ashton, Flinn, Oxnard, and Spence ('73; fig. 21) and McHenry ('72). It is now the contention of both authors of this paper that the principal coordinates analysis is more representative of the actual phenetic affinities of the early hominid pelvic bones : they are hominid in the traits that best distinguish H o m o from extant apes, but they are also unique among the hominoids. Canonical analysis is a desirable multivariate method for some problems because it considers correlation and within-group dispersion, but it can be inappropriate and misleading because it does not take into consideration the uniqueness of the fossils. The two pelvic fragments with no missing data (SK 3155 and Sts 1 4 ) could have been entered as a group into the canonical analysis, and thus not treated as unknowns, but this would make one group with a n inordinately small sample size ( n = 2 ) and would not test the proposition that the two fossils are different from each other. One reason that the results of the principal coordinates analysis of this study differ from some of the results of Zuckerman et al. ('73) is that we have only dealt with those parts of the coxal bone present in
ANALYSIS OF EARLY HOMINID PELVES
SK 3155 (ilium and acetabulum) whereas their study included the ischium and pubis as well. The ischium unfortunately is missing in SK 3155 and badly damaged in both SK 50 and Sts 14. Robinson ('72) has proposed that the ischium of SK 50 is significantly more pongid-like than that of Sts 14. However, Lovejoy et al. ('73) and McHenry ('72, '73) have contested this view: variability is very high in the position of the ischial tuberosity in man and the relative total length of the ischium of SK 50 is not significantly different from Homo sapiens. The implied assumption in this study is that the shape of the ilium and acetabulum is closely related to the function of the hip; similarity in shape is presumably associated with the biomechanical demands of gait. In this regard the shape of the hip of the early hominids including the new fossil found at Swartkrans is most like that of Homo sapiens but with certain differences, It is the differences in shape between the hip joint in Homo sapiens and the early hominids that call for functional interpretations. Some interpretations have been offered recently by other authors (Lovejoy et al., '73; Zihlman and Hunter, '73; Robinson et al., '72; Robinson, '72; McHenry, '74) on the basis of the Makapansgat, Sterkfontein, and the original Swartkrans (SK 50) pelvic fragments. Further study is needed to interpret the new Swartkrans coxal bone. Investigations based on the biomechanical analysis of human bipedalism and the locomotion of other hominoids are the subject of another study in progress. ACKNOWLEDGMENTS
We thank C. K. Brain, P. V. Tobias, M. D. Leakey, R. E. F. Leakey and M. H. Day for permission to study the original fossils; R. Thorington, B. Lawrence, C. Mack, and W. W. Howells for the use of the comparative primate material in their care; and the Wenner Gren Foundation for Anthropological Research for financial support. LITERATURE CITED Blackith, R. E., and R. A. Reyment 1971 Multivariate Morphometrics. Academic Press, London and New York. Boyce, A. J. 1964 The value of some methods of numerical taxonomy with reference to homi-
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noid classification. Systematics Association Publication Number 6, Phenetic and Phylogenetic Classification, pp. 47-65, London. Brain, C. K. 1973 A new hominid bone from Swartkrans. Bull. Transvaal Museum, 14: 13. Brain, C. K., E. S. Vrba and J. T. Robinson 1974 A new hominid innominate bone from Swartkrans. Ann. Transvaal Museum, 29: 55-63. Corruccini, R. S. 1972 Allometry correction i n taximetrics. Syst. Zool., 21: 375-383. 1973 Size and shape i n similarity coefficients based on metric characters. Am. J. Phys. Anthrop., 38: 743-754. 1974 Multivariate analysis i n biological anthropology: some considerations. J. Hum. Evol., 4: 1-19. Day, M. H. 1969 Femoral fragment of a robust australopithecine from Olduvai Gorge, Tanzania. Nature, 221 : 230-233. 1971 Postcranial remains of Homo erectus from Bed IV, Olduvai Gorge, Tanzania. Nature, 232: 383-387. Day, M. H., and B. A. Wood 1968 Functional affinities of the Olduvai Hominid 8 talus. Man, 3: 440-455. Gower, J. C. 1966 Some distance properties of latent root and vector methods used i n multivariate analysis. Biometrika, 53: 326-339. Howells, W. W. 1973 Cranial variation in man. Papers of the Peabody Museum, 67: 1-259. Kowalski, C. J. 1972 A commentary on the use of multivariate statistical methods in anthropometric research. Am. J. Phys. Anthrop., 36: 119-132. Lovejoy, C. O., K. G. Heiple and A. H. Burstein 1973 The gait of Australopithecus. Am. J. Phys. Anthrop., 38: 757-780. McHenry, H. M. 1972 The postcranial skeleton of early Pleistocene hominids. Ph.D. Thesis, Harvard University, Cambridge, Massachusetts. 1973 Australopithecine anatomy. Book review of Early Hominid Posture and Locomotion by J. T. Robinson. University of Chicago Press, Chicago. 1974 The ischium and hip extensor mechanism i n human evolution. Paper presented at the 73rd Annual Meeting of the American Anthropological Association, Mexico City. 1975 A new pelvic fragment from Swartkrans and the relationship between the robust and gracile australopithecines. Am. J . Phys. Anthrop., 43: 245-262. Mosimann, J. E. 1970 Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. J. Amer. Statist. Assoc., 65: 930-945. Oxnard, C. E. 1972 Some African fossil foot bones: A note on the interpolation of fossils into a matrix of extant species. Am. J. Phys. Anthrop., 37: 3-12. 1973 Some inferences from morphometrics: problems posed by uniqueness and diversity among the primates. Syst. Zool., 22: 409424. Oxnard, C. E., and P. M. Neely 1969 The descriptive use of neighborhood limited classification in functional morphology: An analysis
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of the shoulder in primates. J. Morph., 129: 127-148. Robinson, J. T. 1972 Early Hominid Posture and Locomotion. University of Chicago Press, Chicago. Robinson, J. T., L. Freedman and B. A. Sigmon 1972 Some aspects of pongid and hominid bipedality. J. Human Evol., 1: 361-369. Schultz, A. H. 1936 Characters common to higher primates and characters specific for man. Quart. Rev. Biol., 1 1 : 259-283 and 425-455. Sokal, R. R., and P. H. A. Sneath 1963 Principles of Numerical Taxonomy. Freeman, San Francisco.
Zihlman, A. L. 1969 Human locomotion: A reappraisal of the functional and anatomical evidence. Ph.D. Thesis, University of California, Berkeley. 1970 The question of locomotor differences i n Australopithecus. 3rd Int. Congr. Primat., Zurich. Zihlman, A. L., and W. S . Hunter 1972 A biomechanical interpretation of the pelvis of Australopithecus. Folia Primat., 18: 1-19. Zuckerman, S . , E. H. Ashton, R. H. Flinn, C. E. Oxnard and T. F. Spence 1973 Some locomotor features of the pelvic girdle in primates. Symp. 2001. Soc., London, 33; 71-165.
KEY W O R D S Australopithecine . Pelvis . Bipedalism . Multivariate analysis. ABSTRACT Multivariate analyses of the acetabular and iliac parts of fossil hominid and extant hominoid pelvic bones show that ( 1 ) the best preserved fossil from Swartkrans (SK 3155) is more similar to the Sterkfontein pelvis (Sts 14) than either fossil is to any extant hominoid species; ( 2 ) of the living hominoids, all of the fossils are closer to modem Homo snpiens than to the apes; and ( 3 ) the robust and gracile forms of South African australopithecines are somewhat different from one another, the gracile form falling nearer to Homo sapiens, but neither form demonstrably closer to the pongids. Although the hip joint of the gracile form of early hominid is fairly well known, little information has been available about the pelvis of the robust australopithecine. Now that a new pelvic fragment (SK 3155) has been discovered (Brain, '73; McHenry, '75), the possibility exists to assess further the relationship among the early hominids and modern Homo sapiens. Divergence of opinion exists on the relationship between different kinds of fossil early hominids. The new pelvic fragment from Swartkrans can help in the resolution of this problem. The purpose of this paper is to assess the phenetic relationship of the new Swartkrans pelvic fragment through the method of multivariate analysis. This is only one step in the full analysis of the fossil, but it is a valuable undertaking in view of the disparity of opinion on early hominid locomotion (Robinson, '72; Lovejoy et al., '73; Zihlman, '69; Day, '69; Day and Wood, '68; Oxnard, '73) and the difficulty in deriving objective interpretations of fossil postcrania due to the wide variability of extant hominoid species. In the preceding article the senior author presented a traitby-trait discussion of the new pelvic fragment in comparison with other hominoids. In this paper we attempt to synthesize this information into a "total morphological pattern" through multivariate analyses which we feel is an essential step toward AM. J. PHYS. ANTHROP.,43: 263-270.
drawing coherent, objective conchsions by treating the traits as part of a single covarying complex. The hominid fossils used have all been thoroughly described (Robinson, '72; McHenry, '72, '75; Brain et al., '74). They include the new pelvic fragment from Swartkrans (SK 3155) thought to be a member of the robust australopithecine group (Paranthropus or Australopithecus robustus) by McHenry ('72, '75). One fossil classified as Paranthropus or Australopithecus robustus is included (SK 50). Three fossil pelvic fragments of the taxon Australopithecus or Homo africanus (Sts 14, MLD 7, and MLD 25) are included. Olduvai Hominid 28 (Day, '71) is treated in a separate analysis since only a small subset of our measurements is possible on this fossil. MATERIALS AND METHODS
Variability in postcranial morphology is considerable in apes and Homo. In order to obtain some appreciation of the range of variation in the shape of hominoid Felves a comparative sample was measured. The sample is presented in table l of the preceding article (McHenry, '75). Sixteen measurements were taken as described in the previous article. Many numerical techniques exist for analyzing data such as these. Multivariate 263
264
HENRY M. McHENRY AND ROBERT S. CORRUCCINI
statistical methods, such as D2 and canonical variates, have been most popular in the past in anthropology. However, it has become increasingly apparent that these have a number of drawbacks (Oxnard, ’72; OXnard and Neely, ’69; Kowalski, ’72; Blackith and Reyment, ’71). Perhaps foremost among these drawbacks is that the method is not designed to consider single isolated specimens, such as a fossil of unknown affinities, unless that specimen can be assumed to be a member of one of the reference samples of extant species. Thus discriminant function analysis cannot be used to construct natural groupings, as it assumes they are known beforehand. In addition, sample sizes should be approximately equal and each sample size should exceed the number of variables employed (Corruccini, ’74). Formal statistical requirements, such as covariance homogeneity between samples and multivariate normality of distribution, are assumed to be met. Finally, discriminant function loadings seem not always to be trustworthy for interpretation (Howells, ’73). Thus there are difficulties in applying conventional multivariate analysis to individual fossils, especially when they are fragmentary, although the approach remains valuable in problems involving large samples of relatively closely related populations (e.g., extant Homo sapiens skeletal populations, Howells, ’73). Nevertheless, we shall employ canonical variates analysis to compare its results with other methods. We shall employ a simpler, non-parametric approach to reduction and ordination of measurements. The procedure follows these steps : ( a ) First each measurement is standardized by its range to insure equal weight in each variable. ( b ) A n attempt is made to adjust for within-group allometric influences, the distortion of shape by size. It is desirable to eliminate size variability as it is expressed within highly variable or sexually dimorphic species. The procedure involves correction of non-linear tendencies shown between each measurement and the standard size reference variable (Corruccini, ’72), the average magnitude of all measurements in a specimen (Mosimann, ’70). The allometry correction coefficient is a modi-
fied logarithmic coefficient of regression: averaged within Gorilla, Pongo, and Pan. ( c ) To eliminate size effects, measurements are converted to shape variables (Corruccini, ’73). This procedure resembles taking ratios between selected pairs of measurements. The problem with ratios is interpreting their variability: is the divisor increasing or the dividend decreasing? It is preferable to convert each measurement into a ratio of a single, stable variable: the standard size reference variable (Mosimann, ’70). ( d ) The shape variables are used to find distance coefficients between each pair of taxa. This distance is the square root of the average squared difference between variables in standard deviation units, the “Pythagorean”straight-line distance between points in the 16-dimensional space defined by our 16 measurements. The overall shape similarity is thus reduced to a single measure. All subjects are used in this calculation including the fossils. ( e ) Patterns followed by the shape distances are determined through cluster analysis. We employed an agglomerative clustering procedure - two taxa sharing the smallest distance coefficient join into the first cluster, their distances being averaged to the rest of the unclustered points. Then the next closest taxon joins, or another close pair may form a new cluster. The process continues until all points belong to a single cluster. The particular technique we follow is the weighted pair-group method (Sokal and Sneath, ’63). The classification process is heirarchic and does not indicate whether a point is actually intermediate between two groups -it has to join one or the other. ( f ) Cluster analysis is supplemented by principal coordinates analysis, a technique of “scaling” the distances onto axes that may be graphed, giving a plot of relationships that preserves as accurately as possible the original distances between points. Successive coordinates represent diminishing amounts of the total variance; often the first few are sufficient to indicate all the significant factors of variability. Visual assessment of natural groupings of points as they are projected onto principal coordinates can be compared with the cluster analysis.
ANALYSIS O F EARLY HOMINID PELVES
( g ) The contribution of each original measurement to the multivariate pattern of relationships can be estimated through principal component analysis. This technique is a “dual” to principal coordinates analysis (Gower, ’ 6 6 ) , in that it produces identical results in terms of distance scaling when entering variables are standardized. Principal component analysis operates on the p x p matrix of correlations between variables rather than the n x n matrix of distances between objects, finding axes (eigenvectors) of maximum variance. The resulting principal component eigenvector loadings can be converted to factor loadings, or to correlation coefficients between each variable and the component axis. Thus variables showing high correlation with a principal axis, and making a major contribution to the multivariate variation along it, can be detected. The use of these techniques in combination allows the mapping of metric variability in a reduced number of dimensions, reducing the many original raw measurements into a few shape factors. The techniques are essentially free of constraints of statistical theory and parameters, contrasting with classic multivariate statistical analyses such as canonical analysis. A canonical analysis is performed, however, for the purpose of checking the results derived by these other methods.
265 Horn0
S l i 14
MLO 7
MLO 25
SK 50
SK 3155
bp Pang0
Gorilla Hylobaies
Fig. 1 Dendrogram depicting the results of the cluster analysis described in the text. Note the fundamental bifurcation between non-human pongids and hominids (including all of the fossil hominids). Note also that the fossils classified as Australopzthecus or Homo africanus cluster together. The two specimens from Swartkrans are further removed from Homo sapiens t h a n are the gracile australopithecines.
the primary, secondary and tertiary divisions. The first bifurcation occurs between apes and hominids, entirely consistent with oFinions based upon visual inspection of primate pelves: the human shape is quite distinctive especially in its low and broad RESULTS iliac blade. All of the fossil coxal fragments The preceding article (McHenry, ’75) cluster with the human group. The second discusses the univariate pattern of varia- division on the human side is between the tion in the measurements. It is our opinion Swartkrans fossils and the rest of the that a full understanding of the pelvic bone hominids. As figure 1 illustrates, the fossils cannot derive solely from the particulate classified as “gracile” australopithecines presentation of each trait. The analysis of (Azistralopithecus or Homo africanus) all characteristics combined into multivari- cluster very tightly. ate analyses is a necessary addition toward The pongids form three clusters in this the complete understanding of the prob- analysis: Hylobntes, Gorilla and the two lem. The correlations and meaning of each genera, Pan and Pongo. It must be rememvariable presented in table 2 will therefore be discussed in terms of the multivariate bered, of course, that only the acetabulum and ilium are being considered in this analyses to be described below. The dendrogram displayed in figure 1 analysis. The wide separation of Gorilla is represents the results from the cluster not surprising considering the very wide analysis. As is true of other attempts to ilium of this genus. A more precise view of relationships depict the results of muhivariate analyses, the dendrograrn can be deceptive: Boyce can be gleaned from the similarity coeffi(’64) and many others have discussed this cients. Again, the fossil hominids are closer point. What is interesting in figure 1 are to Homo than to any ape (except for the
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HENRY M. McHENRY AND ROBERT S. CORRUCCINI
crushed and distorted SK 50 which is about equally distant from all extant hominoids). The new Swartkrans pelvic fragment is closest to SK 50, but not far from the other fossils. Caution is advised in the interpretation of this result since several crucial variables in the analysis are missing in SK 50, MLD 7 and MLD 25. This fact may influence the results concerning the very close relationship of the two Makapansgat specimens to each other and to Sts 14. One result is quite clear from the similarity coefficients: none of the fossil hominids shows a close relationship with any extant ape. The two Makapansgat specimens are nearest to modern man, while Sts 14 is next closest. The two Swartkrans fossils are considerably more distant from modern man in shape. The results of the principal coordinates analysis are eminently interpretable in terms of function of the hip joint (figs. 2 , 3, table 1 ) . The first principal coordinate accounts for about half of the total variance. Homo and the fossil hominids are widely separated from the rest of the hominoids. There is no overlap in ranges between Homo and the pongids as shown in figure 3 and the two best preserved fossils (Sts 14 and SK 3155) are very close to the
------SK
5
Fig. 2 Stereogram of the first three principal coordinates with coordinate 1 forming the axis from left to right, coordinate 2 forming the axis from front to back, and coordinate 3 forming the vertical axis.
GORILLR GDRILLil PONGO PYGIIQEUS
PRN TROGLODYTES
-
HYLOBRTES LRR
nonn
SRPIENS
SK 3155
STS 14
-\.?'
P R I N C I P R L C O l l P O N E N l ONE
Fig. 3 Range plot of the first principal coordinate. The bars include the actual range of variation on the first coordinate. Note the total separation of Homo and the pongids. Also note that on this important axis (explaining the majority of the total variance) that the two most complete fossils are very far removed from the apes and are close to the humans.
human range. The variables with high correlations with this vector are just those traits that are distinctively human : the ilium is low in Homo sapiens as it is in the fossil hominids; the distances from the center of the acetabulum to the auricular surface of the sacrum and to the posterior superior spine are small; the width of the ilium just above the acetabulum is large; the sacral surface measured as the distance between posterior iliac spines is not high; the acetabulum is deep and large; the acetabulum forms less of an angle with the ilium; the ilium is thicker in the region of the iliac pillar; and the width of the auricular surface is large. The relative width of the ilium is not nearly as important in this differentiation as the iliac height, corroborating Schultz's ('36) observation that hominid ilia were not really relatively widened so much in evolution as they were shortened. In almost all of these distinctively human characteristics the fossil hominids are like Homo sapiens. The only differences are in the size of the acetabulum which is intermediate in early hominids, and the width of the sacral articular surface which is very small in the early hominids relative to other pelvic dimensions. In sum, in the traits that best distinguish the human and ape acetabulum and ilium, the fossil hominids are distinctively
267
ANALYSIS OF EARLY HOMINID PELVES TABLE 1
Principal component loadings converted to factor coefficients which measure the relative importance of each measurement t o each axis Measurement Percent contribution
1 Htacet Transacet Wd post acet Wd ant acet Ht ilium Wd ilium 7 Min wd ilium 8 Thick ilium 9 Thick sciatic 10 Acet-postsup 11 Acet-iliop 12 Antsup-iliop 13 Antsup-postinf 14 Postsup-postinf 15 Postinf-iliop 16 Depth acet 2 3 4 5 6
Component 1
Component 2 17.7
Component 3 14.8
- 0.81 - 0.29 - 0.28 - 0.52
- 0.23
0.26 0.76 0.82 - 0.72 0.13 0.66 0.05 - 0.48 - 0.53 0.10 - 0.05 0.15 0.29 - 0.28 - 0.36 - 0.13
56.8
1.00 - 0.64 - 0.95 -0.81 - 0.65 1.oo
0.95 - 0.30 - 0.83 0.95 - 0.74 - 0.92
human except in being intermediate in the size of the acetabulum and i n the size of the sacral articular surface. The second principal coordinate is concerned with the uniqueness of the early hominid coxal fragments. On this axis Homo sapiens projects at one extreme and the fossil hominids spread out toward the opposite extreme. The variables that are highly correlated with this vector are those that describe the uniqueness of the early hominid pelves : the iliac fossa is peculiarly wide in the fossils (antsup-iliop) and the acetabulum is small. The two Swartkrans specimens project quite high on this axis but the position of SK 50 must be viewed with caution since i t is so badly distorted especially in some of these critical dimensions that distinguish the early hominids from Homo. The gracile australopithecine specimens (Sts 14, MLD 7, MLD 25) fall exactly intermediate on coordinate 2 between Homo sapiens and the Swartkrans specimens. As the first principal coordinate is concerned with the separation of hominids from the rest of the hominoids, the third principal coordinate involves the maximum division of Gorilla and Hylobates with the rest of the hominoids (including all of the hominids) falling half way between. Traits with high correlations with this axis include the width of the ilium, exceptionally large in Gorilla relative to the other vari-
- 0.56 - 0.44
- 0.20
0.08 0.42 - 0.06 0.27 - 0.21 0.08 - 0.22 0.97 0.42 0.05 - 0.43 - 0.06
ables but very narrow in Hylobates, the thickness of the bone in the region of the sciatic notch, relatively thin in Gorilla, the width of the iliac fossa ( antsup-iliop), wide in Gorilla, width of the auricular surface (postinf-iliop), relatively narrow in Gorilla compared to Hylobates, and a number of other traits. The higher coordinates account for diminishingly small amounts of the total variance. They appear to be unimportant and also uninterpretable. Figure 4 presents the first two canonical variates. Only those fossils with the entire suite of measurements are entered by necessity (SK 3155 and sts 1 4 ) . The results are similar to those found by McHenry ('72) : the first canonical variate explains the majority of the variance and acts to separate the hominids from the other hominoids. The two fossils fall with the hominids, but interestingly, SK 3155 is closer to Homo than is Sts 14. The second canonical variate separates Hylobates from Gorilla as did the third principal coordinate. The overall results are similar to the results of the principal coordinates analysis except the uniqueness of the fossils is not shown. This is to be expected since the fossils are not entered into the calculations of the canonical space but are entered as unknowns after the space is defined. Results of principal coordinates and cluster analyses of six measurements of
HENRY M. McHENRY AND ROBERT S. CORRUCCINI
St: 14 SK q155 Homa
'
Ponga
G a p
CANONICAL VARIATE
ON€
Fig. 4 Canonical analysis of the 16 coxal measurements. Note the primary bifurcation between hominids and pongids. Canonical axis I accounts for 72% of the total discrimination and axis I1 accounts for 21.5%.
Olduvai Hominid 28 (Day, '71) show how much more similar this H o m o erectus fossil is to H o m o sapiens than it is to any of the other early hominid fossils. The coefficient of similarity between H o m o sapiens and O.H. 28 is 1.18 compared to 1.40, 1.53, and 1.57 for H. sapiensSK3155, H . sapiens-Sts 14, and H . sapiens - SK 50, respectively. The similarity coefficient between O.H. 28 and SK 3155 is large (1.52), reconfirming the conclusion reached by visual inspection that the new Swartkrans fossil should not be placed in the H o m o erectzis taxon (McHenry, '75). All of the australopithecines were more similar to each other than to either H o m o sapiens or the pongids. DISCUSSION
The results of both the principal coordinates and canonical analyses show that the early hominid ilium and acetabulum are quite unpongid-like. The second principal coordinate is especially interesting in this respect: it shows that the fossils do differ from H o m o sapiens but in a phenetic direction that is independent of or at right angles to the pongid phenetic directions. Despite the australopithecine differences, they share with m a n the whole multivariate
complex which differentiates pongids from hominids. Unlike some studies (e.g., Zihlman, '70; Lovejoy et al., '73) the results here show that the gracile and robust australopithecines are somewhat different in the shape of the iliac blade and the acetabulum. Of particular interest are the differences in the relative width and shape of the iliac blade. As Robinson ('72) has pointed out on SK 50, the robust australopithecines have a characteristically broad and anteriorly expanded iliac blade which is expressed to a lesser extent in the gracile forms (Sts 14, MLD 7 and 25). Caution is required in the interpretation of SK 3155, of course. since the anterior suDerior iliac spine had to be reconstructed.- Its reconstruction was done very conservatively, however, using Sts 14 as a model (where the spine is not so beaked) as well as SK 50. The results of the canonical analysis here are similar to one of those done by Zuckerman, Ashton, Flinn, Oxnard, and Spence ('73; fig. 21) and McHenry ('72). It is now the contention of both authors of this paper that the principal coordinates analysis is more representative of the actual phenetic affinities of the early hominid pelvic bones : they are hominid in the traits that best distinguish H o m o from extant apes, but they are also unique among the hominoids. Canonical analysis is a desirable multivariate method for some problems because it considers correlation and within-group dispersion, but it can be inappropriate and misleading because it does not take into consideration the uniqueness of the fossils. The two pelvic fragments with no missing data (SK 3155 and Sts 1 4 ) could have been entered as a group into the canonical analysis, and thus not treated as unknowns, but this would make one group with a n inordinately small sample size ( n = 2 ) and would not test the proposition that the two fossils are different from each other. One reason that the results of the principal coordinates analysis of this study differ from some of the results of Zuckerman et al. ('73) is that we have only dealt with those parts of the coxal bone present in
ANALYSIS OF EARLY HOMINID PELVES
SK 3155 (ilium and acetabulum) whereas their study included the ischium and pubis as well. The ischium unfortunately is missing in SK 3155 and badly damaged in both SK 50 and Sts 14. Robinson ('72) has proposed that the ischium of SK 50 is significantly more pongid-like than that of Sts 14. However, Lovejoy et al. ('73) and McHenry ('72, '73) have contested this view: variability is very high in the position of the ischial tuberosity in man and the relative total length of the ischium of SK 50 is not significantly different from Homo sapiens. The implied assumption in this study is that the shape of the ilium and acetabulum is closely related to the function of the hip; similarity in shape is presumably associated with the biomechanical demands of gait. In this regard the shape of the hip of the early hominids including the new fossil found at Swartkrans is most like that of Homo sapiens but with certain differences, It is the differences in shape between the hip joint in Homo sapiens and the early hominids that call for functional interpretations. Some interpretations have been offered recently by other authors (Lovejoy et al., '73; Zihlman and Hunter, '73; Robinson et al., '72; Robinson, '72; McHenry, '74) on the basis of the Makapansgat, Sterkfontein, and the original Swartkrans (SK 50) pelvic fragments. Further study is needed to interpret the new Swartkrans coxal bone. Investigations based on the biomechanical analysis of human bipedalism and the locomotion of other hominoids are the subject of another study in progress. ACKNOWLEDGMENTS
We thank C. K. Brain, P. V. Tobias, M. D. Leakey, R. E. F. Leakey and M. H. Day for permission to study the original fossils; R. Thorington, B. Lawrence, C. Mack, and W. W. Howells for the use of the comparative primate material in their care; and the Wenner Gren Foundation for Anthropological Research for financial support. LITERATURE CITED Blackith, R. E., and R. A. Reyment 1971 Multivariate Morphometrics. Academic Press, London and New York. Boyce, A. J. 1964 The value of some methods of numerical taxonomy with reference to homi-
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noid classification. Systematics Association Publication Number 6, Phenetic and Phylogenetic Classification, pp. 47-65, London. Brain, C. K. 1973 A new hominid bone from Swartkrans. Bull. Transvaal Museum, 14: 13. Brain, C. K., E. S. Vrba and J. T. Robinson 1974 A new hominid innominate bone from Swartkrans. Ann. Transvaal Museum, 29: 55-63. Corruccini, R. S. 1972 Allometry correction i n taximetrics. Syst. Zool., 21: 375-383. 1973 Size and shape i n similarity coefficients based on metric characters. Am. J. Phys. Anthrop., 38: 743-754. 1974 Multivariate analysis i n biological anthropology: some considerations. J. Hum. Evol., 4: 1-19. Day, M. H. 1969 Femoral fragment of a robust australopithecine from Olduvai Gorge, Tanzania. Nature, 221 : 230-233. 1971 Postcranial remains of Homo erectus from Bed IV, Olduvai Gorge, Tanzania. Nature, 232: 383-387. Day, M. H., and B. A. Wood 1968 Functional affinities of the Olduvai Hominid 8 talus. Man, 3: 440-455. Gower, J. C. 1966 Some distance properties of latent root and vector methods used i n multivariate analysis. Biometrika, 53: 326-339. Howells, W. W. 1973 Cranial variation in man. Papers of the Peabody Museum, 67: 1-259. Kowalski, C. J. 1972 A commentary on the use of multivariate statistical methods in anthropometric research. Am. J. Phys. Anthrop., 36: 119-132. Lovejoy, C. O., K. G. Heiple and A. H. Burstein 1973 The gait of Australopithecus. Am. J. Phys. Anthrop., 38: 757-780. McHenry, H. M. 1972 The postcranial skeleton of early Pleistocene hominids. Ph.D. Thesis, Harvard University, Cambridge, Massachusetts. 1973 Australopithecine anatomy. Book review of Early Hominid Posture and Locomotion by J. T. Robinson. University of Chicago Press, Chicago. 1974 The ischium and hip extensor mechanism i n human evolution. Paper presented at the 73rd Annual Meeting of the American Anthropological Association, Mexico City. 1975 A new pelvic fragment from Swartkrans and the relationship between the robust and gracile australopithecines. Am. J . Phys. Anthrop., 43: 245-262. Mosimann, J. E. 1970 Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. J. Amer. Statist. Assoc., 65: 930-945. Oxnard, C. E. 1972 Some African fossil foot bones: A note on the interpolation of fossils into a matrix of extant species. Am. J. Phys. Anthrop., 37: 3-12. 1973 Some inferences from morphometrics: problems posed by uniqueness and diversity among the primates. Syst. Zool., 22: 409424. Oxnard, C. E., and P. M. Neely 1969 The descriptive use of neighborhood limited classification in functional morphology: An analysis
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of the shoulder in primates. J. Morph., 129: 127-148. Robinson, J. T. 1972 Early Hominid Posture and Locomotion. University of Chicago Press, Chicago. Robinson, J. T., L. Freedman and B. A. Sigmon 1972 Some aspects of pongid and hominid bipedality. J. Human Evol., 1: 361-369. Schultz, A. H. 1936 Characters common to higher primates and characters specific for man. Quart. Rev. Biol., 1 1 : 259-283 and 425-455. Sokal, R. R., and P. H. A. Sneath 1963 Principles of Numerical Taxonomy. Freeman, San Francisco.
Zihlman, A. L. 1969 Human locomotion: A reappraisal of the functional and anatomical evidence. Ph.D. Thesis, University of California, Berkeley. 1970 The question of locomotor differences i n Australopithecus. 3rd Int. Congr. Primat., Zurich. Zihlman, A. L., and W. S . Hunter 1972 A biomechanical interpretation of the pelvis of Australopithecus. Folia Primat., 18: 1-19. Zuckerman, S . , E. H. Ashton, R. H. Flinn, C. E. Oxnard and T. F. Spence 1973 Some locomotor features of the pelvic girdle in primates. Symp. 2001. Soc., London, 33; 71-165.
