A Female Homo erectus Pelvis from Gona, Ethiopia

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Science  14 Nov 2008:
Vol. 322, Issue 5904, pp. 1089-1092
DOI: 10.1126/science.1163592


Analyses of the KNM-WT 15000 Homo erectus juvenile male partial skeleton from Kenya concluded that this species had a tall thin body shape due to specialized locomotor and climatic adaptations. Moreover, it was concluded that H. erectus pelves were obstetrically restricted to birthing a small-brained altricial neonate. Here we describe a nearly complete early Pleistocene adult female H. erectus pelvis from the Busidima Formation of Gona, Afar, Ethiopia. This obstetrically capacious pelvis demonstrates that pelvic shape in H. erectus was evolving in response to increasing fetal brain size. This pelvis indicates that neither adaptations to tropical environments nor endurance running were primary selective factors in determining pelvis morphology in H. erectus during the early Pleistocene.

The modern human pelvis is uniquely modified to accommodate both bipedal locomotion and the birthing of large-brained offspring (1, 2). The earliest known fossil hominid adult pelves are from small-bodied females (such as the 3.2-million-year-old Australopithecus afarensis specimen A.L. 288-1an/ao and the ∼2.5- to 2.8-million-year-old Au. africanus specimen Sts14) that show anatomical adaptations to bipedal locomotion yet lack obstetric specializations. By the early Pleistocene, Homo erectus exhibited an absolute and relative increase in brain size, suggesting that the parturition of a large-brained fetus may have imposed novel selection on its pelvis. Few early Homo fossil pelvis fragments exist (3), and it is the 1.53-million-year-old juvenile male skeleton (KNM-WT 15000) from Kenya that has been central in assessing H. erectus pelvic morphology and body shape (4). The transversely narrow pelvis and torso reconstructed for this individual were suggested to be adaptations that enhanced locomotor effectiveness and thermoregulatory homeostasis in more open, semi-arid tropical environments (4, 5). Estimates of female birth canal dimensions based on this fossil have been interpreted to suggest that H. erectus lacked derived obstetric modifications in the pelvis and that its small birth canal limited neonatal brain size (3, 6) to a maximum of ∼230 ml. This, in turn, was argued to have resulted in the birth of developmentally immature offspring that experienced rapid postnatal brain growth requiring a modern human–like degree of maternal investment and child-rearing behaviors (6).

Here we describe a nearly complete early Pleistocene adult female H. erectus pelvis and last lumbar vertebra (BSN49/P27a-d) from the upper Busidima Formation (7, 8), dated 1.8 to <0.16 million years ago (Ma), in the Gona Paleoanthropological Research Project study area in the Afar Regional State, Ethiopia (Fig. 1). The BSN49 site is stratigraphically located between the Silbo Tuff (0.751 ± 0.022 Ma) and the base of the C1r polarity chron (1.778 Ma) (fig. S1). Consideration of the range of observed sediment accumulation rates in the Busidima Formation narrows the likely age of the fossil to 0.9 to 1.4 Ma (8). To date, H. erectus is the only hominid known from the early Pleistocene deposits in the Afar Depression. Early Acheulean artifacts are common at the BSN49 stratigraphic level. Analyses of carbon and oxygen stable isotopes from pedogenic carbonates and herbivore enamel from the BSN49 level indicate a semi-arid environment with a landscape dominated by C4 grasses and grazing herbivores (8).

Fig. 1.

Location of site BSN49. See (8) for additional information on site stratigraphy and tuff geochemistry.

The pelvis (Fig. 2) includes the sacrum and both os coxae with the first complete pubis from the early Pleistocene. Most of its distortion was produced by in situ fracture and carbonate cementation of the displaced fragments. The complete pelvis was reconstructed from high-resolution plaster casts. Despite minor residual asymmetry, the major functionally relevant dimensions and articular surfaces required little or no reconstruction and can be considered reliable for anatomical interpretation and mensuration (8).

Fig. 2.

Illustrations of major elements of the BSN49/P27 pelvis and lumbar vertebra and reconstruction of the pelvis. (A) Right os coxa with posterolateral view of the ilium and anterolateral view of an ischiopubic fragment. (B) Anterior and posterior views of the sacrum. (C) Right lateral view of the lumbar vertebra. (D) Posterolateral view of the left ilium and anterolateral view of the left ischiopubic fragment. (E) Right lateral view. (F) Left lateral view. (G) Anterior view. (H) Posterior view. (I) Pelvic inlet. (J) Pelvic outlet. The blue portions of the cast indicate areas that have been reconstructed or restored. Scale bar for (A) to (D), 40 mm; scale bar for (E) to (J), 200 mm.

The adult BSN49/P27 pelvis is transversely broad with laterally flaring ilia and anteriorly positioned acetabulocristal buttresses, long pubic rami, and a wide sciatic notch, which are all plesiomorphic characters shared with the australopithecines, other early (3) and middle (9, 10) Pleistocene Homo, and Neandertals (11). The fossils attributable to H. erectus or early Homo [including KNM-WT 15000, KNM-ER 1808, KNM-ER 3228, OH28, and UA-173/404+UA-466 (3, 12)] span the early Pleistocene in Africa and exhibit laterally flaring ilia, wide (in terms of modern males) greater sciatic notches, tall thin pubic symphyseal faces, small auricular surfaces, and anteriorly placed iliac pillars. Except for overall size, the BSN49/P27 specimen is anatomically similar to these pelvis fossils (8). The BSN49/P27 pelvis shares with Homo such diagnostic characters (8) as an anteroposteriorly broadened birth canal, a thickened acetabulocristal buttress (iliac pillar), a sigmoid-shaped anterior inferior iliac spine, a shelf formed by attachment of the reflected head of the rectus femoris muscle, deepened fossa for the gluteus medius muscle, an increased height of the posterior ilium with an expanded retroauricular area, and angular elevation and anterior projection of the superior pubic rami (13). As in other Homo sacra, the BSN49/P27 alae are anteroposteriorly broad with marked periauricular excavation and a robust and projecting sacral tuberosity indicating a well-developed interosseous sacroiliac ligament complex: features that readily distinguish Homo from the australopithecines (8).

The BSN49/P27 acetabulae are small, with an estimated femoral head diameter of 33.4 to 36.8 mm (8)—substantially smaller than the femoral head of other early Pleistocene specimens [such as KNM-WT 15000: 44.9 mm (14)]. Regressions estimating femur length and stature based on the major load-bearing articular surfaces of the pelvis (8) predict a stature for the BSN49/P27 individual of 1.20 to 1.46 m, markedly shorter than the 1.85 m adult stature estimated for the male KNM-WT 15000 individual (4). Although H. erectus is widely characterized as apomorphically exhibiting an increase in stature and reduction in stature dimorphism, the data supporting this idea are surprisingly meager. With the recent discovery of H. erectus crania and postcrania from smaller individuals [such as KNM-OL 45500 (15), KNM-ER 42700 (16), and Dmanisi (17, 18)], it is apparent that body size range in H. erectus has been underestimated, and a size “Rubicon” should not be part of the species diagnosis (16). The presence of very wide greater sciatic notches (8) and subpubic angle (table S5), everted ischia, rectangular pubic bodies with a ventral arc, a subpubic concavity, a large sacral angle (19), a nonprojecting sacral promontory, a symmetrically oval pelvic inlet, and a preauricular sulcus are all traits diagnostic of a female pelvis. Thus, the BSN49/P27 pelvis is from a short-statured H. erectus adult female.

The BSN49/P27 pelvis is obstetrically capacious for such a short-statured individual. The fossil's inlet circumference is within modern female ranges (8). The obstetrically important bispinous (pelvic midplane) and bitubercular (pelvic outlet) transverse breadths of BSN49/P27 are greater than in most modern females (Fig. 3) (8). Size-normalized comparisons and multivariate analyses of the pelvic inlet and midplane demonstrate the obstetrically derived shape of the BSN49/P27 birth canal (Fig. 3, C and D) (8).

Fig. 3.

Comparative pelvimetrics. (A) Plot of acetabulum superoinferior diameter with the square root of the sacral S1 body area (8). (B) Plot of bituberous breadth (pelvic outlet breadth) and bispinous breadth (pelvic midplane breadth). (C) Anteroposterior (AP) and mediolateral (ML) birth canal inlet dimensions normalized by acetabulum superoinferior diameter. (D) Anteroposterior and transverse birth canal midplane dimensions normalized by acetabulum superoinferior diameter. Human data are from The Hamann-Todd collection, Cleveland Museum of Natural History, Cleveland, Ohio. Open inverted triangles, females; gray triangles, males; black diamond, BSN49/P27.

Humans are unusual among the hominoids in having a near identity in size between the neonatal head and the birth canal dimensions that places both mother and neonate at substantial risk of a traumatic birth. When these anatomical relationships in humans were used to estimate neonatal head size in H. erectus, it was seen that the BSN49/P27 pelvis was capable of birthing an offspring with estimated maximal brain volume of up to 315 ml (8)—over 30% greater than previously predicted from the KNM-WT 15000 pelvis (6), although this value is similar to growth-based estimates (20). Neonatal brain size was approximately 30 to 50% (the mean ratio is 34 to 36%) of early Pleistocene H. erectus adult brain size [∼600 to 1067 ml (mean = 880 ml, n = 18 crania)] (21), an intermediate value between that of chimpanzees (∼40%) and modern humans (∼28%) (20). This new estimate of H. erectus neonatal brain size, in tandem with the revised age at death (∼0.5 to 1.5 years) of the child's cranium from Perning (Mojokerto), Indonesia (<1.81 Ma) (22), suggests that H. erectus had a prenatal brain growth rate similar to that of humans but a postnatal brain and somatic growth rate intermediate between that of chimpanzees and humans (23).

The enlarged neonatal brain in H. erectus required a concomitant increase in the dimensions of their bony birth canal. Two nonexclusive means of enlarging birth canal size beyond the primitive Australopithecus condition (1) are an increase in female body size [larger females can have isometrically larger pelves (24)] or developmentally mediated changes in pelvic shape resulting in pelvic sexual dimorphism. Given this individual's short stature with a capacious birth canal and characteristically female pelvic shape, it is clear that the latter applies. This resulted in a recognizably dimorphic pelvis by the early Pleistocene, with females demonstrating the distinctive obstetric anatomy required to deliver a large-brained offspring. This derived anatomy indicates that the fetal cephalic–maternal pelvic disproportion, which directly affects reproductive success, was a significant selective factor on female pelvic morphology at that time.

This individual's absolutely wide bi-iliac breadth (288 mm) is greater than the mean width of modern females and males from eight diverse populations (8, 19, 25, 26), indicating that the BSN49/P27 individual had a very broad trunk. Its bi-iliac breadth is exceeded in the fossil record only by the very large middle and late Pleistocene pelves from Atapuerca, Spain (9), Jinniushan, China (10), and Kebara, Israel (11), which are specimens that retain the primitive condition of laterally flaring ilia. The only ancient pelvis that does not exhibit marked lateral flare is the reconstructed KNM-WT 15000 pelvis, a reconstruction that has been questioned (3, 9).

Many anatomical changes in the human pelvis have occurred since the middle Pleistocene, including a narrowing of the interacetabular distance; an increase in the anteroposterior breadth of the birth canal, with shorter, elevated pubic rami; and a decrease in the degree of iliac flaring, leading to a reduction of the bi-iliac breadth (13). Some authors have suggested that these anatomical adaptations had their roots in the early Pleistocene as a locomotor adaptation by H. erectus to endurance running (5). The BSN49/P27 pelvis does not exhibit any of these anatomical modifications or others proposed to be adaptive responses to this behavior, such as tall stature, enlarged acetabulae, or a narrow torso. Clearly, improving locomotor effectiveness, as exhibited by a relative and absolute increase in lower limb length, was a component of the early Homo adaptive complex. However, the earliest fossil evidence of the modern human pelvis is documented about 100,000 years ago from Skhul, Israel, indicating both the recency of this morphology and the historical stability of the plesiomorphic transversely broad pelvis.

Modern humans display a relation between body shape and ambient temperature and humidity, with individuals living in more temperate and Arctic climates having absolutely and relatively broader torsos, and peoples in tropical arid/semi-arid areas possessing narrower trunks (27). The BSN49/P27 pelvis represents a short-statured, broad-hipped individual who would have had an extreme bi-iliac breadth/stature ratio characteristic of more temperate-adapted modern humans and not the tall narrow body form previously identified in H. erectus as an adaptation to tropical semi-arid environments (4, 8). Thus, although early Homo lived in a diversity of environments, because of their unique pelvic shape they did not exhibit the same ecogeographic patterns of body form as seen in modern humans (10).

The first H. erectus fossils were found over 100 years ago. Additional H. erectus remains have since been recovered from numerous sites spanning over a million years, thousands of miles, and a wide diversity of ecological zones. These fossils have documented a substantial increase in endocranial capacity in H. erectus over their Pliocene ancestors. Despite this rich history, few complete fossil postcrania (18) have been recovered, and basic features of H. erectus body shape remain poorly understood. The transversely broad torso, clearly evident in this short individual, requires reappraisal of some current models of locomotor and ecogeographic adaptations in African early Pleistocene H. erectus. It is now clear that the H. erectus pelvis retained many elements of its australopithecine heritage, although substantially modified by the demands of birthing large-brained offspring.

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Tables S1 to S10


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