When did the modern human pattern of childbirth arise? New insights from an old Neandertal pelvis

Human birthing is difficult owing to a tradeoff between large neonatal brain size and maternal pelvic dimensions, which are constrained by aspects of bipedal biomechanics (1, 2). The net effect is that human neonatal head size closely matches maternal pelvic dimensions, unlike in our closest living relatives, the great apes, whose pelvic dimensions are larger than neonatal head sizes. This size relationship, along with a twisted birth canal shape, makes human parturition mechanically difficult and results in a unique pattern of “rotational” birth (Fig. 1). As in humans, and unlike great apes, monkey neonatal head size closely matches the mother's pelvic dimensions. Although birth rotation occurs in some monkeys, the rotation pattern is different from that in modern humans, with monkey neonates exiting the birth canal facing forward (1). Therefore, in both apes and monkeys, it is relatively easy for a mother to guide her infant out of the birth canal, keep the umbilical cord from wrapping around the neck, and extract mucous from the nose and mouth to facilitate breathing. All of these critical activities are much more difficult for a human mother, whose infant emerges facing backwards, and pulling on the infant from this position also risks serious neck injury. For these reasons, humans uniquely engage in assisted birth (obligate midwifery). Although unassisted birth, the norm for nonhuman primates, does occasionally occur in humans, assisted birth and its myriad social implications are the human norm cross-culturally (1).

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Fig. 1.

The human birth canal inlet (a) is larger transversely (side to side) than it is anteroposteriorly (front to back) because bipedal efficiency favors a shorter anteroposterior distance between a line that passes through both hip joints (d) and the sacrum (e). The human neonatal head is longer from front to back (Lower) and therefore enters the transversely wider birth inlet (a) facing sideways (Upper). As the neonate enters the pelvic midplane (b), which is anteroposteriorly wider, its head rotates 90° to accommodate the twisted birth canal, and faces backwards away from the pelvic pubic bones (Lower) while its transversely wide and relatively rigid shoulders are accommodated by the wider inlet. The baby then exits its mother's body facing backwards, turning slightly sideways again as its shoulders align to pass through the anteroposteriorly wider midplane and outlet (c). This figure was prepared by Nathan Holton, University of Iowa. [Upper reproduced with permission (Copyright 2009, Corbis). Lower reproduced with permission (Copyright 2009, Nucleus Medical Art).]

Obstetrical difficulties and some form of birthing assistance may have arisen at the outset of hominin evolution in concert with bipedalism (3), yet it seems likely based on 2 preserved Pliocene female pelves, A.L. 288-1 (Australopithecus afarensis) and Sts 14 (Australopithecus africanus), that birth in australopiths was nonrotational, with the long axis of the neonate's head oriented transversely as it moved through the 3 birth canal planes (2). The extant human pattern of rotational birth, along with intensified and obligate midwifery, most likely emerged later when a critical threshold of brain size attainment in Homo was added to the shared hominoid pattern of broad, rigid shoulders (4). But when did this happen?

Until now, the consensus has been that rotational birth was not present in Early Pleistocene Homo (5), recently confirmed by the discovery of a largely complete 1.4–0.9 million-year-old female Homo erectus pelvis from Gona, Ethiopia (6), with the primitive nonrotational pattern persisting until the Middle Pleistocene (5). Resolving the appearance of rotational birth more precisely has been hindered by the paucity of fossil pelvic remains, especially from females, because of the fragility of pelvic bones. In a recent issue of PNAS, Weaver and Hublin (7) report on a virtual reconstruction of the pelvis of the Tabun C1 adult female Neandertal which indicates, surprisingly, that Neandertals retained the primitive birth pattern into the Late Pleistocene, and that the shift to a rotational birth pattern occurred later in human evolution than previously thought.

Over the past 25 years, rotational birth has been inferred for archaic Homo sapiens based largely on 3 specimens (3): Sima 1, a 600,000-year-old male pelvis from the Sima de los Huesos, Spain (8, 9); a 260,000-year-old left os coxa belonging to a partial female skeleton from Jinniushan, northeastern China (10, 11); and a 60,000-year-old partial pelvis from a male Levantine Neandertal, Kébara 2 (12). Nonetheless, it has always been recognized that extrapolating female birth canal shape from male pelvic remains is uncertain. Moreover, whereas the inlet anatomy of the female Jinniushan specimen can be estimated (11), the midplane and outlet dimensions are unknown.

For these reasons, Weaver and Hublin have returned to a fossil discovered nearly 80 years ago. The Tabun C1 pelvis belongs to a 60,000- to 100,000-year-old female Neandertal skeleton and was partially reconstructed and described in 1939 (13). Her pelvic remains consist of portions of the left pubis and ilium, as well as the right pubis, ischium, and ilium. The advent of computerized virtual reconstruction allows highly accurate restorations of fragmented and variably distorted fossil elements, including mirror imaging of damaged or missing elements. The Weaver and Hublin reconstruction is actually the second modern-day effort. In a 2008 study in PNAS assessing Neandertal neonatal brain size and subsequent brain growth relative to recent modern humans to compare life history rates, Ponce de Léon and colleagues (14) produced a virtual reconstruction of the Tabun C1 pelvis and used it to simulate the birth process in Neandertals by using a complete neonatal skeleton from Mezmaiskaya Cave, Russia (15). In their reconstruction of the Tabun C1 pelvis, Ponce de Léon and colleagues argued that the midplane and outlet configuration could not be established from the fossil elements alone because of an inability to accurately infer the ischial and sacral orientations. Consequently, they assumed the modern human rotational pattern for the Mezmaiskaya neonate and modern human cephalopelvic proportions to parameterize the reconstructed birth dimensions.

Weaver and Hublin (7) focus on parturition itself, and they ask whether Neandertal females, represented by the Tabun C1 pelvis, actually had the same birth canal size and shape proportions as recent humans, and thus rotational birth, which was assumed in the Ponce de Léon et al. (14) study. After computed tomography scanning the original pelvic fragments, Weaver and Hublin first virtually “disassembled” portions of the original 1939 reconstruction and separated the femoral head from the right acetabulum; the heads of both the right and left femora were cemented so firmly within the hip joints that the original describers (13) never attempted to separate them. After this step, Weaver and Hublin mirrored missing elements on the left side from the more complete right side elements, and then fit and aligned the elements from each side of the pelvis by using both manual and computer algorithm techniques. They then used an E-M (expectation-maximization) program to estimate crucial missing points such as those from the nonexistent sacrum. Finally, the more complete right side of the pelvis was mirrored to create the left side.

The resulting birth inlet and outlet areas of Tabun C1's reconstructed pelvis are very similar to the mean area value for a geographically diverse sample of recent modern female pelves compiled by the authors. The surprising result, however, was that for birth canal shape. Tabun C1's inlet index (anteroposterior breadth/transverse breadth) at 0.79 is low compared with recent human females, and her outlet index at 0.70 is extremely low, in fact, falling entirely out of the range of Weaver and Hublin's extensive comparative sample. Compared to the characteristically anteroposteriorly oval outlet in modern humans (index values >1.0, Fig. 1 Lower), Tabun C1's outlet is transversely oval. Although poor preservation of the ischial spine precludes definitive assessment of the midplane, the results for the outlet shape in Tabun C1 indicate that Neandertals had a different birthing pattern from modern humans. Rather than rotating so that the head is anteroposteriorly oriented (facing away from the mother, Fig. 1 Lower), Neandertals would have aligned their heads transversely exiting through the birth outlet. The authors test the veracity of their results against 2 key potential sources of reconstruction error: the estimation of the sacral landmarks, and the orientation of the pubis fragment relative to the hip joint and other elements of the hemipelvis by using a variety of compelling corroboratory techniques.

Neandertals had a different birthing pattern from modern humans.

What do the divergent Neandertal and extant modern human birthing patterns imply? Despite its male attribution, Sima 1 best represents pelvic shape in the last common ancestor of Neandertals and humans (9), and it has been used to infer neonatal midplane rotation (8). Weaver and Hublin raise caveats about that interpretation, but note that all agree on a transversely oval outlet in Sima 1. They argue that Middle Pleistocene encephalization trends (16) increased obstetric constraints in both the Neandertal and modern human lineages with divergent results. Neandertals continued to expand transverse pelvic outlet dimensions (the primitive condition), commensurate with large bi-iliac breadths and cold adaptation, with secondary consequences such as more or less equal pubic bone lengths in both Neandertal sexes (10). Modern humans, in contrast, underwent anteroposterior expansion of the birth outlet, since the African ancestors of modern humans were built on a transversely narrow pelvis bauplan related to warmer climate. The new wide-hipped female Homo erectus pelvis from Gona (6) complicates this climatic explanation, but does provide evidence for continuity in wide bi-iliac breadths from Australopithecus to Neandertals. New interpretations of the thorax in Neandertals mirrors this continuity by postulating that a wide body with high body mass represents the primitive hominin condition retained in Neandertals, which, if related to cold adaptation, represented an exaptation rather than cold adaptation per se (17). Finally, as Weaver and Hublin (7) acknowledge, the differences in the precise birthing pattern between Neandertals and modern humans should not let us lose sight of the fact that both lineages would have had difficult births, obligate midwifery, and all of the attendant social implications.