Implications of allometry
The tests for isometry reveal that positive allometry is a factor in PCA of all taxa and of all apes, suggesting that some of the shape variation discussed below is due to size differences among taxa. Analyses of Pan–Gorilla, and of Pongo, Pan and Hylobates individually, appear to be free of allometric effects, while Gorilla exhibits positive allometry. Positive allometry is not surprising in the analysis of all taxa and all apes because the body mass of hylobatids, and in particular Hylobates lar, is much lower than that of the other included taxa (Smith & Jungers, 1997). Although the size of the femora under comparison is a factor, the phenetic results show that overall, small-bodied gibbons are similar to large-bodied orangutans, and relatively small-bodied chimpanzees are most similar to large-bodied gorillas. This observation indicates that all of the identified shape variation is not due to size (Oxnard, 1978), although the current results do not allow precise discrimination between aspects of shape that are size-related and size-independent. The size-related shape variation described below is functionally important and is desirable to discuss (Jungers & Susman, 1984; Jungers, 1988).
Comparative femoral shape among taxa
Together, the results show that the morphology of quadrupedal/climbing African apes is different from that of suspensory/climbing Asian apes, suggesting that locomotor category is a good predictor of ape femoral shape. Femoral shape in Homo and Pongo is broadly similar, which is not predicted on the basis of their different locomotor categories. The relationship between shape variation, locomotor categories and taxon is summarized in Table 5.
Table 5. Shape characteristics of the proximal femur by locomotor category and taxon. Shape is partitioned into discrete characters based on PCA and TPSA
|Large superiorly projecting head|
|Long neck between head and greater trochanter|
|Greater trochanter superoinferiorly short, mediolaterally expanded|
|Posteriorly projecting intertrochanteric crest|
|Long neck between head and greater trochanter||Intertrochanteric crest does not project posteriorly|
|Greater trochanter superoinferiorly short||Pongo|
|Head projects superiorly relative to the head||Large head|
|Posteriorly projecting intertrochanteric crest|
|Small nonsuperiorly projecting head||Head mediolaterally short|
|Short neck between head and greater trochanter||Trochanteric fossa shallow|
|Greater trochanter superoinferiorly long, mediolaterally narrow||Lesser trochanter and intertrochanteric crest inferiorly placed|
|Posteriorly projecting intertrochanteric crest||Pan|
|Head mediolaterally long|
|Trochanteric fossa deep|
|Lesser trochanter and intertrochanteric crest superiorly placed|
The relative position of the greater trochanter and head, and the configuration of the greater trochanter distinguish suspensory/climbing Asian apes from quadrupedal/climbing African apes. The superoinferior length of the greater trochanter is short in Hylobates and Pongo, and is longer in Pan and Gorilla. In the predominately suspensory/climbing apes, the superior end of the greater trochanter is positioned lower than the femoral head. The functional outcome of the relative position of the head and greater trochanter in Asian apes is greater hip mobility, as described below. High neck-shaft angle has been invoked to explain the superior projection of the head of Pongo (Lovejoy et al. 2002). The results here show how this morphology might be achieved. In Asian apes, the distance between the centre of the neck and the border of the head and neck is longer than in African apes, which appears to contribute to the superior projection of the head relative to the greater trochanter. In the predominately quadrupedal/climbing apes, the superior aspects of the femoral head and greater trochanter are at the same level, or the greater trochanter may project above the head. Although it is unclear what, if any, significance this arrangement has for locomotion, there may be some advantage for extension of the thigh (Preuschoft, 1970). In Pan this muscle is engaged in extension as well as medial rotation in climbing (Stern & Susman, 1981).
As demonstrated in the cluster analysis phenogram (Fig. 2), the shape of the bipedal proximal femur is most similar to that of Asian apes, and Pongo in particular. The small number of landmarks in this study suggests that cautious interpretation of the similarities between Homo and Pongo is warranted. Pongo and Homo have comparatively large femoral head diameters, superiorly projecting heads, longer necks and short greater trochanters. The shared shape of Pongo and Homo is likely to be convergent, resulting from similar adaptive solutions for bipedality, on the one hand, and climbing, on the other. Independent evolution is supported by the absence of a ligamentum teres in Pongo, which promotes joint mobility, and presence of this feature in humans, which promotes joint stability.
A locomotor pattern of bimanual suspension and quadrumanual climbing can explain much of the femoral anatomy of Pongo (Schaffler et al. 1985; Ruff, 1987, 1988; MacLatchy & Bossert, 1996; Ruff, 2002). The relatively large femoral head is consistent with analyses by Ruff (2002) and Godfrey et al. (1995), demonstrating that climbers, in contrast to predominately quadupedal primates, have larger hindlimb joint surface areas relative to diaphyseal strength. Although not empirically demonstrated, the shorter greater trochanter of Pongo could relate to the gluteus minimus configuration. The orangutan gluteus minimus is separated into gluteus scansorius (a thigh flexor, abductor and medial rotator), and the gluteus minimus proper, which medially rotates and abducts the thigh (Sigmon, 1974). According to Sigmon, the effect of the divided gluteus minimus is enhanced freedom of movement at the hip joint, which is adaptive for quadrumanual climbing. The two muscle insertions in orangutans, rather than the single, linear insertion in other apes, could explain the shorter greater trochanter (Sigmon, 1974; Aiello & Dean, 1990). That the head is above, rather than below, the greater trochanter in Pongo relates to joint mobility, as a lower greater trochanter interferes less with abduction of the thigh (Aiello & Dean, 1990).
Most aspects of the proximal femoral shape of Homo relate to bipedal locomotion. The short superoinferior extent of the greater trochanter can be associated with the proportionately smaller percentage of hip musculature that comprises gluteus medius and minimus in Homo (Stern, 1972; Sigmon, 1974; Stern & Susman, 1983). These muscles attach on the lateral and anterior aspects of the greater trochanter, and thus define the anteroposterior and superoinferior dimensions of this feature. In apes the deeper gluteals involve a greater percentage of the overall gluteal musculature (Stern, 1972; Sigmon, 1974; Stern & Susman, 1983). Although not directly demonstrated, the low position of the greater trochanter relative to the head may be the developmental outcome of the bipedalism-induced valgus knee (Tardieu & Preuschoft, 1996; Tardieu & Damsin, 1997). It is also likely that this arrangement enhances the action of the abductors in stabilizing the stance-phase hip during bipedal progression (Lovejoy et al. 2002).
The shape of the proximal femur in Hylobates is not greatly different from that of Pongo and Homo. It would be interesting to determine whether, with the inclusion of other gibbon taxa and siamangs, the common Asian ape pattern of proximal femoral shape holds. Shape differences that exist between Hylobates and other taxa are demonstrably influenced by size. Hylobates is distinguished from other taxa primarily by a very slight intertrochanteric crest and an inferiorly positioned lesser trochanter. The slight intertrochanteric crest of gibbons, compared with the more exaggerated version in other taxa, is likely to be an allometric effect. The intertrochanteric crest is the point of insertion for the quadratus femoris, a lateral thigh rotator and abductor (Sigmon, 1974). Sigmon reported that Hylobates musculature is long and slender in comparison with that of great apes. This characteristic, which is perhaps related to body size, could explain the lack of intertrochanteric crest robustness in gibbons.
Comparative femoral shape among African apes
This analysis reveals morphological similarity between Gorilla and Pan, which is consistent with their common locomotor mode of quadrupedal knucklewalking and climbing. There are some shape differences between Pan and Gorilla, such as in the shape of the head and its relationship to the neck, the depth of the trochanteric fossa, and the position of the intertrochanteric crest relative to the head. The larger articular surface in the Pan femoral head is linked to the capability for a significant degree of abduction at the hip joint (MacLatchy & Bossert, 1996; MacLatchy, 1996). In Gorilla, the articular surface is less mediolaterally deep, suggesting a more limited capacity for abduction. In keeping with this morphology and with larger body size, G. g. gorilla reportedly climbs much less often than does Pan (Gebo, 1996).
Pan has a very deep trochanteric fossa that is not shared by Gorilla. The deep trochanteric fossa has been attributed to a large insertion of the lateral thigh rotator, obturator externus (Aiello & Dean, 1990). By contrast, Lovejoy et al. (2002: 107) argued that the unusually deep trochanteric fossa of Pan is a ‘developmental-modeling feature’ of no biomechanical or phylogenetic consequence. Thus, it remains unclear why Pan would be exaggerated in this regard relative to Gorilla.
That Pan and Gorilla are knucklewalkers, but at very different body sizes, is an explanation for the differences in joint morphology, yet intergeneric allometry is not detected in this analysis. Lovejoy et al. (2002: 115) found differences between Pan and Gorilla in their analysis of a few characters and few specimens, and as explanation, suggested sampling factors, differential adaptation, morphological drift or body size effects. The discrete attributes of Pan and Gorilla joint morphology, which cannot easily be attributed to allometry in this analysis of numerous specimens, eliminates sampling effects and body size effects as plausible explanations. Better explanations for the differences between Pan and Gorilla lie in their different behaviours, which are probably the consequence of substrate-use constraints imposed on large-bodied gorillas (Gebo, 1996).
In most analyses gorillas are widely dispersed across axes of variation, suggesting that they are highly variable in proximal femoral shape. One potential source of the variation is between the subspecies G. g. gorilla and G. g. beringei, which might be more appropriately considered separate species (Groves, 2001; Grubb et al. 2003). Differences between them have been identified in the cranium and mandible, the distal humerus, and in the femoral head surface area (Lague & Jungers, 1999; Ruff, 2002; Guy et al. 2003; Taylor & Groves, 2003). Although G. g. gorilla and G. g. beringei are differentiated from one another in the cluster analysis based on all variation, the difference was not reflected in the significant principal components. The test for intrageneric isometry reveals an allometric relationship among gorillas, which could relate to the presence of the two subspecies. Sexual dimorphism is another possible explanation, although allometry is not detected among similarly sexually dimorphic orangutans.
Implications for the evolution of the proximal femur
The results have implications for the evolution of the proximal femur. Vertical climbing, such as practised by orangutans, has been identified as a pre-adaptation for bipedalism (Stern & Susman, 1981; Fleagle et al. 1981). Therefore, shape similarities in Homo and Pongo could be primitive characters not found in African apes owing to their derived quadrupedal knucklewalking adaptation. The observation that Hylobates shares a relatively long neck, a short greater trochanter and a superiorly projecting head with Pongo and Homo indicates that these features could be primitive traits. Although Hylobates engages in leaping and bipedal walking and Pongo in arboreal quadrupedalism (Fleagle, 1976; Sugardjito & van Hooff, 1986; Cant, 1987), Asian apes are mainly suspensory and infrequently load their hindlimbs (Schaffler et al. 1985; Ruff, 1987), suggesting that locomotor pattern is an equally plausible explanation for their shared morphology. If the last common ancestor of African apes and humans was a quadrupedal knucklewalker (e.g. Richmond et al. 2001), it could be argued that the femoral morphology of chimpanzees and gorillas represents the ancestral state for the African ape and human clade, and that femoral shape in humans converges on that of Asian apes, whose morphology is primitive.
At least three evolutionary scenarios are consistent with the identified pattern of shape: (1) femoral shape in Pongo and Hylobates is primitive, while African ape morphology and that of Homo are secondarily derived, either independently or from a common ancestor; (2) the morphology of African apes is primitive, while that of Hylobates, Pongo and Homo developed independently in response to locomotor requirements; and (3) femoral morphology in each lineage evolved independently and the morphology of the last common ancestor of all apes remains elusive. These alternatives cannot be completely evaluated without consideration of additional hindlimb elements. At least for the proximal femur, function, rather than phylogeny, is likely to make the greater impact on shape.