Nearly 20 genera of ‘hominoids’ are currently known from the Miocene of Africa (Fleagle, 1999); but taxonomy of Hominoidea is controversial (see, e.g. Harrison, 2002, for a different perspective). Among Early Miocene hominoids, the anatomy of the postcranium is best known in the 17–20 Ma genus Proconsul, owing to the existence of several partial skeletons as well as many isolated specimens (Napier & Davis, 1959; Harrison, 1982; Walker & Pickford, 1983; Beard et al. 1986; Senut, 1986; Gebo et al. 1988; Ward et al. 1991, 1993, 1995; Begun et al. 1994).
Table 1 summarizes the major postcranial features of Proconsul. Most of them are obtained from two species of Proconsul, a smaller species, P. heseloni and a larger, P. nyanzae. The thoracic cage is transversly narrow as in most mammals (Ward, 1993). Living apes, however, have a transversely wide thorax, an important adaptation for suspension or climbing (Schultz, 1961; Erikson, 1963; Gebo, 1996). Lumbar vertebrae have a moderately long centrum (Ward et al. 1993) and their transverse processes arise from the body at the pedicle roots (Ward et al. 1993). This condition differs from that in living apes, in which the transverse process arises from the pedicle (Sanders & Bodenbender, 1994). The lumbar region is reduced in extant suspensory specialized primates, even in some New World monkeys (Schultz, 1961; Erikson, 1963). The lumbar vertebrae number six or more in Proconsul (Ward et al. 1993), greater than in living apes (in which it is mostly 3–5). Thus, the lumbar region of Proconsul is long, like that of Old World monkeys. It is arguable whether or not Proconsul had lost the tail (positive assessments in Ward et al. 1991, 1999; negative in Harrison, 1998). However, a recent analysis supports tail loss (M. Nakatsukasa et al., unpubl. data). The pelvis is narrow, as is the thorax (Ward, 1993) and Proconsul lacked ischial tuberosities (Ward et al. 1993) unlike Old World monkeys and gibbons (Rose, 1974). Neither forelimb nor forearm is very long (Napier & Davis, 1959). The humerus does not have medial torsion of the head (Walker, 1997), and although it is unclear whether the proximal humeral shaft is curved or not, sharp deltopectoral and deltotriceps crests are developed as in the humeri of Old World monkeys (Napier & Davis, 1959). The humeral trochlea is not truly trochleiform, although the lateral trochlear keel is relatively well developed in P. heseloni (Napier & Davis, 1959; Senut, 1986). The ulna articulates with the triquetral and pisiform (Napier & Davis, 1959; Beard et al. 1986). The pollex and hallux are well developed (Harrison, 1982; Begun et al. 1994) unlike in living hominoids in which they are diminutive. However, phalanges lack a pronounced curvature (Napier & Davis, 1959; Harrison, 1982; Begun et al. 1994). Hand and foot phalanges cannot be distinguished easily (Begun et al. 1994; Nakatsukasa et al. 2003a). In summary, Proconsul lacks most of the postcranial specializations for suspensory positional behaviour, which are observed in living apes (see Larson, 1998).
Table 1. Major postcranial features in Proconsul
|Thoracic cage is mediolaterally narrow (Ward, 1993)|
|Lumbar vertebrae have a long centrum (Ward et al. 1993; Rose et al. 1996); small cranial/caudal articular surfaces (Harrison & Sanders, 1999; Nakatsukasa & Hirose, 2002) and transverse processes arising from the body at the pedicle roots (Ward et al. 1993). Lumbar vertebrae number six or more (Ward et al. 1993)|
|Tail loss controversial (positive: Ward et al. 1991, 1999; negative: Harrison, 1998)|
|Narrow ilium and sacrum; no ischial tuberosities (Ward, 1993)|
|Neither forelimb nor forearm is elongated (Napier & Davis, 1959; Walker & Pickford, 1983)|
|No strong humeral head torsion (Walker, 1997)|
|Developed deltopectoral/deltotriceps crests (Napier & Davis, 1959)|
|Humeral trochlea is not truly trochleiform, lacking a developed lateral keel (Napier & Davis, 1959; Senut, 1986)|
|Ulna articulates with the triquetral and pisiform (Napier & Davis, 1959; Beard et al. 1986)|
|Well-developed pollex and hallux; phalangeal curvature is not pronounced; II–V phalanges are generally similar between hand and foot (Napier & Davis, 1959; Harrison, 1982; Begun et al. 1994)|
Middle and Late Miocene
During the early phase of the Middle Miocene, roughly between 13 and 15 Ma, several new hominoid species appeared in Africa, such as Nacholapithecus, Kenyapithecus and Otavipithecus (Le Gros Clark & Leakey, 1951; Leakey, 1962; Pickford, 1985; Conroy et al. 1992; McCrossin, 1994; Ishida et al. 1999). The genus Kenyapithecus includes two species, wickeri and africanus (Pickford, 1985; McCrossin, 1994; McCrossin & Benefit, 1997) but there is a proposal to move the latter into a different genus, Equatorius (Ward et al. 1999a,b). Although this proposal is not fully accepted, it is becoming apparent that there was a large diversity of medium-to-large hominoids from southern to eastern Africa during this period (S. Ward et al. 1999).
Recently, plenty of Nacholapithecus specimens have been excavated from Nachola in northern Kenya (Nakatsukasa et al. 1998, 2000; Ishida et al. 1999, 2004). The holotype of Nacholapithecus KNM-BG 35250 (Fig. 1) is one of the most complete hominoid skeletons ever found (Ishida et al. 2004). Thanks to the excavations at Nachola, the postcranial anatomy of Nacholapithecus is now the best known among African fossil hominoids.
Nacholapithecus is a medium-sized hominoid. Body mass in males has been estimated as less than 20 kg, from femoral head size (Nakatsukasa et al. 2000). However, from its large forelimb bones relative to the hindlimb a weight closer to 22 kg has been suggested (Ishida et al. 2004). This would make it about half the size of a common chimpanzee.
Table 2 lists the major postcranial traits of Nacholapithecus. The clavicle is very long: for example, the clavicle of KNM-BG 35250 is about 84 mm long (Sent et al. 2004; Fig. 2). Even if it lacks only the sternal end, the original length would be a minimum of 100 mm. With a body mass that is about a half of that of a common chimpanzee and equivalent to that of a male yellow baboon (Smith & Jungers, 1997), this bone is naturally extremely long: the average length of the clavicle in a male chimpanzee is about 125 mm (Senut et al. 2004). A long clavicle suggests either a laterally projecting glenoid fossa of the scapula (= a wide thoracic cage) or an extremely cranially angled clavicle (= a cranially facing glenoid surface) as is in orang-utans (Fig. 3). Because marked medial torsion of the humeral head does not exist in Nacholapithecus (M. Nakatsukasa, personal observation), the latter interpretation is more probable. If so, this is most likely an adaptation for climbing.
Figure 2. Limb bones of KNM-BG 35250 (casts) compared with those of a male Pan troglodytes schweinfurthii. Note great size of the forelimb bones relative to hindlimb bones in KNM-BG 35250. Scale bar = 5 cm.
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Morphology of the lumbar vertebrae is generally similar to that in Proconsul: for example, non-pedicular origin of the transverse processes, moderate centrum length, vertebral number 6–7 (Rose et al. 1996; Nakatsukasa et al. 1998, 2003b). Curiously, Nacholapithecus has small lumbar vertebral bodies relative to body mass (Nakatsukasa et al. 2003b). If a lumbar vertebra of KNM-BG 35250 is compared with the fourth lumbar vertebra of a male yellow baboon whose femur is equivalent in size to that of KNM-BG 35250, it is evident that the Nacholapithecus vertebra is much smaller (Fig. 4). A similar tendency is observed in Proconsul and may be related to a common and unique locomotor pattern in those hominoids (Nakatsukasa & Hirose, 2003).
Figure 4. Femur and lumbar vertebra of KNM-BG 35250 compared with those of a male baboon (Papio cynocephalus). Although the femoral heads are almost identical in size, the lumbar vertebral centrum of this male Nacholapithecus is much smaller than that of L4 in this baboon. Also note the left transverse process which arises from the body-pedicle juncture in Nacholapithecus. Scale bar = 2 cm.
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Although the axial skeleton of Nacholapithecus lacks most of the derived features observed in living apes, at least one derived feature may be identified with confidence: Nacholapithecus did not have a tail (Nakatsukasa et al. 2003c). Recently, a first coccygeal vertebra of Nacholapithecus was discovered (KNM-BG 40949). This is an almost complete bone despite the erosion of the distal tip (Fig. 5). Although it is slightly elongated compared with that of living hominoids, it shares several important functional features with coccygeal bones of living hominoids, such as the complete absence of vertebral foramina, reduced transverse processes and dorsoventral compression. These features indicate a diminution of voluntary ability to control more caudal elements, a reduction of tail muscles and reduced mobility at the sacrococcygeal joint. The reason for the tail loss was probably slow locomotion coupled with enhanced cheiridial grasping capability (Nakatsukasa et al. 2003a). The overall morphological similarity of the coccyx with that in living apes may suggest that incipient formation of a pelvic floor of the type seen in living apes (Abitbol, 1988) existed in Nacholapithecus, as an adaptation for orthograde postural and locomotor behaviour.
Figure 5. First coccygeal/caudal vertebra in short-tailed or tailless primates. Upper (left to right): Gorilla gorilla, Pan troglodytes, Hylobates syndactylus. Lower (left to right): Macaca nigra, Perodicticus potto, Nycticebus sp., Nacholapithecus. Note the similarity between Nacholapithecus and living hominoids’ coccyges. Scale bar = 2 mm.
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The Nacholapithecus elbow exhibits several derived features. Although the humero-ulnar joint is of a primitive cylindrical type, the lateral wall of the olecranon-fossa is markedly developed (Nakatsukasa et al. 1998, 2000; Takano et al. 2003; Ishida et al. 2004). The humeral capitulum is tall and globular. Probably, the elbow joint was adapted for enhanced pronation–supination through the full range of flexion–extension; Takano et al. (2003) suggest use of a wide range of arboreal supports.
The most curious postcranial feature in Nacholapithecus is its body proportions. Nacholapithecus has forelimb bones that are proportionally large compared with the lumbar vertebrae and hindlimb bones (Nakatsukasa et al. 2000; Ishida et al. 2004). Figure 2 compares limb bones of the Nacholapithecus type specimen (KNM-BG 35250) with those of a male chimpanzee. Although the forelimb bones of KNM-BG 35250 are only modestly smaller than in chimpanzees, its hindlimb bones are much smaller. This is apparent in an allometric plot of the distal joint width of the humerus against femoral head diameter (Fig. 6a). Femoral head size is a robust surrogate for body mass prediction, although it may sometimes yield overestimates of body mass, as it does for example in orang-utans) (Ruff, 1988, 2002). Thus, Nacholapithecus has large forelimb bones, not small hindlimb bones, and probably relied on its forelimbs to a greater degree than do other non-suspensory primates. Differentiation of bone structural strength between the fore- and hindlimb bones by locomotor characteristics is noted in various living anthropoids (Ruff, 2002).
Figure 6. Allometric scaling of postcranial dimensions. (a) Distal joint width of the humerus against the femoral head diameter with least squares regressions for African apes, cercopithecids and cebids. (b) Third digit length against body mass. Nacholapithecus: KNM-BG 35250AQ-AS. Proconsul heseloni: KPS3 ph233, 82, 80. Numeric in the figure corresponds to living taxon as follows. 1: male Ateles seniculus, 2: male Cebus albifrons, 3: male Cacajao calvus, 4: male Pithecia monachus, 5: male Lagothrix lagotricha, 6: male Brachyteles arachnoides, 7: male Cercopithecus mitis, 8: male Papio cynocephalus, 9: male Macaca nemestrina, 10: male Colobus guereza, 11: male Pan troglogytes schweinfurthii, 12: female P. t. verus, 13: male P. t. verus, 14: male P. t. troglodytes, 15: male Gorilla gorilla gorilla, 16: male G. g. beringei.
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Phalanges of Nacholapithecus are generally similar to those of Proconsul in terms of the absence of specialized features for suspension (Rose et al. 1996; Nakatsukasa et al. 2003a). However, Nacholapithecus differs from Proconsul in its phalangeal elongation, enhanced robustness of the hallucial phalanges and greater size of manual phalanges relative to corresponding pedal phalanges (Nakatsukasa et al. 2003a). Figure 7 compares hallucial phalanges of KNM-BG 35250 with those of P. heseloni (KNM-KPS 3). The wider shaft of the proximal phalanx and the broader base of the terminal phalanx in Nacholapithecus are quite distinctive. Figure 6(b) plots pedal third digit length of living anthropoids on body mass bi-logarithmically. A median ray of KNM-BG 35250 is much of a positive outlier as that of the spider monkey (Ateles). Although P. heseloni also has a long pedal digit compared with most anthropoids, the deviation is less marked in this species.
Figure 7. Right hallucial phalanges of Nacholapithecus (KNM-BG 35250) and Proconsul heseloni (KNM KPS 3) in plantar (a) and lateral view (b). Scale bar = 5 mm.
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In summary, the postcranial features suggest that Nacholapithecus engaged in orthograde behaviours (e.g. vertical climbing, hoisting, bridging) more frequently than did Proconsul; it had developed grasping capability, and moved relatively slowly in the trees (Nakatsukasa et al. 2003a). However, the absence of related features in the shoulder and hand imply that suspensory specialization had not developed by this stage.
Locomotor patterns of other contemporary hominoids are less well known. However, owing to discoveries from Maboko Island, Kenya, of K. africanus is an exception. It is proposed that K. africanus had forearm and femoral features related to scansorial activities, including a forelimb-dominated positional repertoire (McCrossin et al. 1998). One of the humeral shafts discovered is straight like that of modern apes. Interestingly, it is suggested that the locomotor repertoire of K. africanus included a significant terrestrial component (McCrossin, 1994; McCrossin & Benefit, 1997; Sherwood et al. 2002). Benefit & McCrossin (1995) argue that the transition from arboreal life to terrestrial life among African large-bodied hominoids originated at this stage. If so, suspensory specialization occurred later than, or simultaneously with, the terrestrial adaptation in later African hominoids. This scenario needs better justification by discoveries of younger fossil material.
By contrast, apparently suspensorily specialized apes had appeared by 12 Ma in Europe (Moyà-Solà & Köhler, 1996). Dryopithecus has long manual phalanges with marked curvature and was apparently adapted for frequent suspension. Slightly older, Sivapithecus, from the Siwaliks, shared derived postcranial features with African apes while retaining primitive catarrhine postcranial features (Rose, 1986, 1993, 1994; Pilbeam et al. 1990; Spoor et al. 1991; Ward, 1997; Madar et al. 2002). Its humerus exhibits shaft curvature (Pilbeam et al. 1990; Richmond & Whalen, 2001) and it is unlikely that suspensory behaviour had a large share in its total positional repertoire. Its phalanges exhibit stronger suggestions of arboreal behaviour than do those of Nacholapithecus (Nakatsukasa et al. 2003a). But like Nacholapithecus it possessed well-developed and large halluces and pollices (Rose, 1994; Madar et al. 2002), which suggests frequent use of a pollex-/hallux-assisted power grip rather than a hook-like hand position. The positional repertoire for Sivapithecus advocated by Madar et al. (2002) is very similar to that of Nacholapithecus, although Sivapithecus was more specialized in many regards. Besides the difference in body size, they probably differed in the proportional contribution of elements of the positional repertoire. However, these two taxa are derived in a similar fashion.
After 13 Ma there is no hominoid postcranial material in Africa until 6 Ma. Probably, suspensorily specialized African hominoid(s) evolved during this period. However, some researchers argue a Eurasian origin of suspensorily adapted hominoids (the ‘Return from Eurasia Hypothesis’; see Stewart & Disotell, 1998; Begun, 2001).
Figure 8 presents a scenario of Miocene hominoid locomotor evolution based on the above ideas. It should be stressed, however, that there is no consensus among researchers concerning Middle to Late Miocene hominoid evolution, and that this schema is not necessarily supported by all evidence currently available.
One of the lumbar vertebrae of Morotopithecus (UMP 67-28) from Uganda at 20.6 Ma has features like those of modern apes, probably reflecting climbing and/or suspensory activity (Walker & Rose, 1968; Ward, 1993; Sanders & Bodenbender, 1994; MacLatchy et al. 2000). The scenario presented relies on the assumption that those modern lumbar features of Morotopithecus are homoplastic. However, it is possible that adaptation for suspensory behaviour in hominoids started in the Early Miocene and that most currently known East African fossil hominoids are members of out-groups, relative to Morotopithecus and extant apes (Gebo et al. 1997; MacLatchy et al. 2000). The similarity between Nacholapithecus and Sivapithecus in evolutionary trends, as well as a lack of suspensorily specialized hominoids on the likely migration route to Europe (e.g. from Turkey), leads me to favour the first possibility (i.e. a Sivapithecus–Pongo clade).
Besides the origin(s) of suspensory adaptation, uncertainties remain about the origins of terrestriality/plantigrady in African apes and humans (e.g. Gebo, 1992; Crompton et al. 2003), and knuckle-walking in African apes. Although Richmond & Strait (2000) found wrist bone features of early hominid fossils that suggest humans evolved from knuckle-walking ancestors, arguments continue (Dainton, 2001; Lovejoy et al. 2001; but see Corruccini & McHenry, 2001; Richmond & Strait, 2001; Richmond et al. 2001). Until timing of these events is defined, many evolutionary scenarios for the antecedents of human bipedality are possible. To test the validity of each scenario, hominoid postcranial material from Africa between 13 and 6 Ma (e.g. Samburu Hills (9.5 Ma), Nakali (9.5 Ma?), Ngeringerwa (9.5–10 Ma) and Ngorora (12.5–10.5 Ma)) would be desirable.