Postcranial morphology of the middle Pleistocene humans from Sima de los Huesos, Spain

Stature.

The mean stature of the SH hominins has been estimated based on 24 complete long bones from the upper and lower limbs (26). The overall stature [(male mean + female mean)/2] of the SH hominins (163.6 cm) is 3.0 cm taller than the mean stature in Neandertals (160.6 cm) (SI Appendix, Table S3).

Body Mass.

Body mass (BM) can be reconstructed from hominin skeletal remains using both morphometric [stature and bi-iliac breadth (BIB)] (29) or mechanical approaches (joint surface size of weight-bearing skeletal elements) (30). The BM of one large male (Pelvis 1 individual) calculated from stature and BIB is between 90.3 and 92.5 kg (25), and the Pelvis 2 individual seems to be slightly broader (Fig. 1A). The pooled sex-weighted mean BM estimated from five adult SH femoral heads is 69.1 kg and is 6.3 kg below the Neandertal mean (75.4 kg) (SI Appendix, Table S4 and Fig. S2).

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Fig. 1.

SH-selected measurements compared with other hominin groups. (A) Bi-iliac breadth. (B) Femoral total length. (C) Femoral head diameter. (D) Femoral neck index (biomechanical length of the neck following ref. 60/femoral maximum length × 100). (E) Percentage of cortical area in the right and left humeri and femora. (F) Palmar projection of the trapezium tubercle. EP1: 2.0–1.8 Mya early Pleistocene Homo; EP2: 1.7–0.8 Mya early Pleistocene Homo; MP: non-SH middle Pleistocene Homo; Ne: Neandertals; MH: modern humans. See SI Appendix for raw data. Boxes: SD; whiskers: range.

Body Shape.

Evidence from the shoulder girdle, the thorax, and the pelvis points to a wide and large body type in the SH hominins. The SH clavicles are absolutely long compared with modern humans (MH), and they show the type II curvature in the coronal plane that is present in all pre-H. sapiens hominins (31). This character has been related to a more lateral and higher position of the scapulae (see below). Regarding the thorax, the absence of complete midthoracic ribs makes it difficult to assess whether the size and shape of the SH costal skeleton is similar to that of Neandertals (32). However, the dorsoventral size of the single complete first rib is longer than MH and Neandertals, and an incomplete second rib suggests that it was dorso-ventrally longer than that of Kebara 2. This suggests that the SH hominins, like Neandertals, had a larger costal skeleton relative to their stature compared with MH (see below). Finally, this population presents very broad elliptical pelves (Fig. 1A) characterized by very wide sacra, pronounced lateral iliac flaring, and long pubic rami that clearly separate it from the MH pelvic configuration (see below).

Intrapopulational Size Variation.

Using a randomization method, relying on bootstrapping, the size variation in the SH hominins was studied as a proxy for their level of sexual dimorphism (33, 34), including additional anatomical parts that were previously underrepresented (SI Appendix, Tables S5–S7). Contrary to previous suggestions that middle Pleistocene humans were more dimorphic (35, 36), the SH hominins do not show an unusual degree of size variation compared with MH.

Different anatomical parts display different levels of variation with between 6.1 and 98.2% of the samples of the same size randomly generated from large samples of MH presenting more variation than in SH. The variation observed in the different anatomical regions may be due to differences in the SH sample sizes depending on the skeletal region, variation in the different modern human samples used, and/or varying correlation of the skeletal regions with overall body size. Thus, sexual dimorphism in SH was not significantly different from the moderate level of sexual dimorphism exhibited by MH. Although there appears to be a somewhat elevated level of intrapopulational variation and sexual dimorphism in the SH sample when we compare the BM values to that of modern humans (SI Appendix, Table S4), this result is based on the still relatively small sample of femoral head estimates (n = 5) in SH. In addition, modern human sexual dimorphism shows some degree of populational variation, and future SH findings may allow for a more precise assessment of this matter.

EQ.

Nine EQ values have been calculated for the SH adult crania (16) using the femoral head diameter (FHD) to calculate BM (SI Appendix, Table S8) and yield a mean EQ of 3.54. The higher EQ of the SH population compared with the published values in the early Pleistocene Dmanisi hominins (37) demonstrates that the increase in brain size in SH was not simply a consequence of an increase in body mass (29). Although the use of the FHD rather than the BIB (see above) yields lower BM values and, consequently, higher EQ values, the EQ from the SH sample is still significantly lower than that of Neandertals (P < 0.003) and MH (P < 0.006). There is a further increase in the EQ in both MH and Neandertals (SI Appendix, Table S8), which suggests that a parallel encephalization process occurred after their last common ancestor (10). Nevertheless, the lower EQ value in the SH population indicates that, in the case of the Neandertals, this brain size increase occurred after the SH population.

Thorax and Spine.

The dorsoventral size of the single SH complete first rib and an incomplete second rib suggest that the SH hominins had a larger costal skeleton relative to their stature compared with MH (SI Appendix, Table S10 and Fig. S3). The atlas displays a large maximum dorsoventral canal diameter (related to the size of the foramen magnum of the SH crania). The axis is craniocaudally low, and the atlantoaxial joint is mediolaterally (ML) expanded (24). The SH hominins show C6 and C7 spinous processes that are more horizontally oriented than in MH and shorter than in Neandertals. At least the L3 and L5 lumbar vertebrae display very long and, unlike the Neandertals, dorso-laterally oriented transverse processes (Fig. 2A and SI Appendix, Tables S11 and S12 and Figs. S3–S5). Finally, the SH hominins show a reduced lumbar lordosis, i.e., a less curved lumbar spine, based on the vertebral wedging in lumbar vertebrae and the incidence of the pelvis, a derived feature shared with Neandertals (25, 38).

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Fig. 2.

SH-selected postcranial traits. (A) Third lumbar vertebra (L3). Cranial view of VL2, presenting a very long and dorso-laterally oriented transverse process (arrowhead). (B) Humerus. Subadult (H-IV, Left) and adult (H-VI, Right) specimens showing the thin medial pillar and broad and deep olecranon fossa. (C) First metacarpal (MC1). Palmar view of juvenile (AT-3104, Left) and adult (AT-5565, Right) specimens, both showing a strong attachment for the opponens pollicis muscle (arrowheads). (D) Os coxae. Ventral view of AT-1000, displaying a strongly twisted anterior inferior iliac spine (white arrow) and a deep iliopsoas groove (black arrow). (E) Femur. F-X (Left) and F-XI (Right) proximal femora in posterior view, showing a low neck angle, large gluteal ridges, and well-developed hypotrochanteric fossae. Midshaft section (Middle, CT-scan image) is rounded and shows an absence of a pilaster. (F) Talus. Dorsal view of AT-2803 that shows an expanded lateral malleolar facet (arrowhead) and parallel edges of the trochlea.

Shoulder Girdle and Upper Limb.

The SH glenoid cavity is consistently taller and narrower (n = 10) than in MH, reflected in a low glenoid index (SI Appendix, Fig. S6 and Tables S13–S16). The SH sample shows a dominant dorsal position (n = 8) of the axillary sulcus for the Musculus teres minor (on the axillary border), resembling the predominant condition in Neandertals. Only one specimen (Scapula IV) displays a ventral sulcus (the most frequent condition in MH).

The curvatures of the SH clavicles in the transverse plane fall within the normal variation in MH. Nevertheless, the curvatures in the coronal plane, in all of the SH specimens where it can be determined, are of type II, as is the case in all Neandertals that we have studied and the few known early Pleistocene specimens. In contrast, MH show three curvature types (31).

Most of the SH humeri display a consistent morphological pattern that distinguishes them from MH and is similar to Neandertals. This pattern includes a transversely oval humeral head, a projected and massive lesser trochanter, a narrower deltoid tuberosity with two muscular crests, thick cortical diaphyses (Fig. 1E), a broader and deeper olecranon fossa, a relatively narrower medial distal pillar surrounding the olecranon fossa (Fig. 2B), a rectangular and broader capitulum, and a shallower trochlea with a less projecting lateral rim. In these two latter traits, the specimens show some variation.

The ulnae have a broader olecranon process, an anterior orientation of the trochlear notch (the plesiomorphic condition for all hominins), a vertically extended radial notch, a short and blunt supinator crest, a robust pronator crest, a blunt interosseous crest, a rounded and gracile diaphysis and pronounced antero-posterior (AP) and ML shaft curvature (SI Appendix, Fig. S7). This pattern is also present in the Neandertals and distinguishes them from MH (SI Appendix, Tables S13–S16).

Most of the SH radii (six of eight specimens) display a relatively long and gracile neck, an antero-medially oriented radial tuberosity, and a low robusticity index with a pronounced ML shaft curvature, as in the Neandertals. However, two SH specimens show the relatively short and robust neck, anteriorly oriented radial tuberosity, and the straight and robust shaft typical of MH (SI Appendix, Fig. S8).

Hand.

The SH hand is characterized by a strong development of the palmar tubercles of the carpal bones associated with a deep carpal tunnel (palmar projections of the tubercle of the trapezium and the hamulus) (Fig. 1F); high mobility of the first metacarpal (MC1), reflected in the saddle-shaped carpo-metacarpal articulation of the thumb; high capacity for rotation of the second metacarpal (MC2); robust thumbs with a strong attachment for the Musculus opponens pollicis (Fig. 2C), relatively short proximal phalanges, and relatively long distal phalanges; noncurved proximal and middle phalanges with relatively broad trochleae; distal phalanges with expanded distal tuberosities; pea-shaped pisiforms; and relatively short (proximo-distal) lunates and relatively broad (radio-ulnar) triquetrals (SI Appendix, Table S17). The SH hand morphology indicates a powerful precision grip and fine precision grasping capabilities that are similar to what has been described in Neandertals (39) and MH. In the SH hand, like in Neandertals, the powerful precision grip is enhanced by the thumb robusticity and well-developed flexor musculature.

Pelvic Girdle and Lower Limb.

The SH pelvises are characterized by their marked robusticity (e.g., large sacroiliac joint, iliac tubercle, and ischial tuberosity) and large overall dimensions. The SH sample shows remarkably broad, tall, and AP-expanded pelvises. The total length of the sacrum and of the complete hip bone, and of the ischium, ilium, and pubis, the vertical acetabular diameter, and the breadth of the ilium and sacrum are conspicuously above MH (SI Appendix, Table S18). The SH pelvic remains are also distinct from MH in having an anteriorly located acetabulocristal buttress, a well-developed supraacetabular groove and a thin and rectangular, plate-like superior pubic ramus that contrasts with the thick and stout pubis of MH (10, 25) (SI Appendix, Figs. S9 and S10). These features, together with the very broad elliptical pelvis, are shared with early and middle Pleistocene Homo specimens, and they likely represent the plesiomorphic condition for the genus Homo.

Neandertals depart from the SH pattern mainly in having an extreme craniocaudal flattening of the pubic ramus (10, 11, 25, 40). Neandertal pelvises, although broader than MH (probably due to prominent iliac flaring), are narrower than SH, likely related to a significantly smaller sacral breadth and iliac height in Neandertals (SI Appendix, Table S18). Unlike MH, the anterior inferior iliac spine (AIIS) of the Neandertals is medially twisted relative to the anterior margin of the iliac blade and is bordered by a deep iliopsoas groove that excavates the medial surface of the AIIS (41, 42). This AIIS configuration agrees with that found in the SH sample (Fig. 2D) and other middle Pleistocene hip bones (43). In contrast, the iliopsoas groove in hip bones of earlier Homo taxa is shallow and does not excavate the medial surface of the AIIS (44).

The SH femora show the plesiomorphic morphological pattern found in most earlier members of the genus Homo (45⇓–47). The SH femora have relatively longer and, on average, moderately AP-flattened necks, ML-widened proximal (subtrochanteric) shaft, relatively low-neck-shaft angle, large gluteal ridges, well-developed hypotrochanteric fossae and proximal lateral crest, absence of a true pilaster, very low point of minimum shaft breadth, and thicker cortical bone than in MH (Figs. 1 D and E and 2E and SI Appendix, Fig. S11 and Tables S19–S22).

The SH tibiae share a similar morphological pattern with Neandertals that includes large retroversion angle of the proximal epiphysis (SI Appendix, Fig. S12 and Tables S19–S22), tibial condyles located in a more posterior position in relation to the axis of the shaft, and flat proximal and distal articular surfaces. Distally, there is moderate hypertrophy of the medial malleolus and presence of squatting facets in some adult specimens (25%), related by some researchers to a hyperdorsiflexion of the ankle joint (48). The robusticity of the fibula overlaps the upper range for MH.

In all of the anatomical details of the upper and lower limb, the SH immature individuals follow the same pattern as in the adult specimens (SI Appendix, Tables S14 and S20).

Foot.

Despite subtle variation in Pleistocene hominin tali, some consistent morphological variants can be identified among different fossil samples (27, 49). The Neandertal talus displays broader lateral malleolar facets (50) and talar heads compared with MH. In the SH specimens, the peroneal facet is significantly broader (Fig. 2F) and the talar head narrower than both Neandertals and MH (SI Appendix, Table S23). In SH, as in Neandertals, the trochlea is relatively broad with parallel sides, compared with the relatively narrow and wedge-shaped trochlea of MH (27, 49) (Fig. 1F). Finally, all Pleistocene (non-H. sapiens) fossil tali, including SH, show a tall trochlea compared with recent MH, allowing for a greater capacity for dorsiflexion and plantarflexion of the ankle joint (51).

The calcanei of Neandertals are broad with a projected sustentaculum tali and a long calcaneal tuber (39). In SH, the calcanei are also broad and the sustentaculum tali is even more projected (28).

The metatarsals from SH, Neandertals, and MH are very similar except for the broader base of the lateral metatarsals (MTIII–V), a potentially derived character shared between SH and Neandertals (49). The SH proximal pedal phalanges present hypertrophy of the shaft, and the distal phalanx of the big toe shows an expanded distal tuberosity, as in the Neandertals (39, 52).