Abstract Hominin birth mechanics have been examined and debated from limited and often fragmentary fossil pelvic material. Some have proposed that birth in the early hominin genus Australopithecus was relatively easy and ape-like, while others have argued for a more complex, human-like birth mechanism in australopiths. Still others have hypothesized a unique birth mechanism, with no known modern equivalent. Preliminary work on the pelvis of the recently discovered 1.98 million-year-old hominin Australopithecus sediba found it to possess a unique combination of Homo and Australopithecus-like features. Here, we create a composite pelvis of Australopithecus sediba to reconstruct the birth process in this early hominin. Consistent with other hominin species, including modern humans, the fetus would enter the pelvic inlet in a transverse direction. However, unlike in modern humans, the fetus would not need additional rotations to traverse the birth canal. Further fetal rotation is unnecessary even with a Homo-like pelvic midplane expansion, not seen in earlier hominin species. With a birth canal shape more closely associated with specimens from the genus Homo and a lack of cephalopelvic or shoulder constraints, we therefore find evidence to support the hypothesis that the pelvic morphology of Australopithecus sediba is a result of locomotor, rather than strictly obstetric constraints.

Citation: Laudicina NM, Rodriguez F, DeSilva JM (2019) Reconstructing birth in Australopithecus sediba. PLoS ONE 14(9): e0221871. https://doi.org/10.1371/journal.pone.0221871 Editor: Karen Rosenberg, University of Delaware, UNITED STATES Received: January 5, 2019; Accepted: August 17, 2019; Published: September 18, 2019 Copyright: © 2019 Laudicina et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the manuscript and its Supporting Information files. 3D surface scans of A. sediba fossil material (U.W. 88-133, U.W. 88-52, U.W. 88-137, U.W. 88-14) are downloadable at www.morphosource.org. Funding: This research was funded by Boston University and Dartmouth College. Competing interests: The authors have declared that no competing interests exist.

Introduction Among primates, the mechanics of human birth are thought to be unique, typically involving a vertex presentation of the fetal head and a multi-rotational pattern of the neonate through the birth canal. The evolutionary explanation for the difficulty of human birth, termed the “obstetrical dilemma” [1], posits that a large, encephalized infant combined with pelvic modifications adapted for bipedality result in an exceeding difficult parturition in humans. In particular, compared to the ape pelvis, the human pelvis is anteroposteriorly (AP) shorter and mediolaterally (ML) broader, which effectively constricts dimensions of the birth canal relative to the modern ape condition. Humans have adapted to the obstetrical dilemma in part by recruiting attendants who aid the mother in giving birth [2, 3]. Although recent research has found that the obstetrical dilemma, as originally conceived, fails to explain the timing of human birth [4–8], it is generally accepted that humans experience more difficult births than do our closest living relatives, the great apes, who typically labor for less time and without the assistance of others [2, 9–12]. Non-human apes achieve this relative ease of parturition through a smaller neonatal size (cranium and body), a more spacious birth canal, and a consistent orientation of the neonate’s head throughout the birth canal [2, 12]. Although variable [9, 13], the majority of ape neonates present in the occiput-posterior position. Thus, the birth process in non-human apes is relatively simple compared to humans. The birth canal and the neonate’s head are elongated in the same plane (anterior-posterior) and the birth canal does not change shape or dimensions [2]. In contrast, the modern human pelvis is shaped in a manner that typically requires fetal rotation, both of the cranium and shoulders [2, 14, 15]. As a human neonate descends into the pelvic inlet, its cranium is aligned obliquely, or transversely, in the birth canal due to the shortened anterior-posterior dimension of the maternal pelvic inlet [2]. Typically, the neonate's head will flex, tucking the chin to its chest, to achieve a shorter length along the suboccipito-bregmatic axis or plane, helping to alleviate the tight fit [2]. In contrast, the AP expanded pelvic inlet of non-human primates allows the neonate to align its head sagittally, without this initial rotation or need for neck flexion [2, 3, 14, 16, 17]. A further constraint is met in the midplane of the human maternal pelvis. The ischial spines constrict the transverse diameter and the anterior-posterior dimension becomes relatively elongated [2, 3, 14, 17]. Taking advantage of the maximum dimensions of the maternal pelvis [18], the neonate's head typically aligns the convex occiput against the complementary surface of the female pubis, resulting in an occiput-anterior birth position [2, 3, 14, 19]. In non-human primates, the occiput-posterior birth position allows the mother to assist the neonate out of the birth canal without risking injury. In humans, the baby is most commonly born occiput-anterior. In this position the mother may extend the neonatal neck, risking spinal injury if she tries to help it out herself [2, 3, 14]. Modern humans have overcome this predicament with birth assistants who aid the newborn safely out of the birth canal. A final challenge that is too often ignored is imposed by the neonatal shoulders. Birth complications due to shoulder obstruction, or shoulder dystocia, occur in 1.4% of the U.S. population [20], of which 24.9% result in fetal injury [21]. Like the neonatal head, the broad, rigid shoulders follow the maximum dimensions of the maternal birth canal [2, 3, 14, 18]. After transverse descent into the inlet, the shoulders twist to be sagittally-aligned with the greatest axis of the maternal pelvis in the midplane. In exiting the birth canal, one shoulder will typically position under the pubic symphysis before the other shoulder, alleviating the tight fit [2, 3, 14]. When rotational birth evolved in hominins is unclear, partially due to the scarcity of female pelvic remains [2, 3, 14, 17, 22–24]. The platypelloid pelvis of the 3.18-million-year-old Australopithecus afarensis skeleton, A. L. 288–1, indicates that an A. afarensis neonate's head would probably have entered the pelvic inlet in a human-like transverse or oblique orientation [15–17, 23, 25, 26]. The Berge et al. [23] reconstruction suggest a more human-like neonatal flexion and rotation through the birth canal while the Tague and Lovejoy [17] reconstruction favors a continued transverse, or asynclitic, passage of the neonate throughout the birth canal. Incorporation of the neonatal shoulder dimensions suggest that a semi-rotational oblique birth would be most probable [15]. Another interpretation posits that this specimen is not a female, given the close fit between a hypothetical A. afarensis neonate and the A.L. 288–1 birth canal [25] (but see [27–29]). Although we do not agree with the conclusion that A.L. 288–1 is a male specimen, obstetric dimensions from both Tague and Lovejoy [17] and Häusler and Schmid [25] are utilized as a range. Hypothesized birth mechanisms of A. africanus are similarly contentious based on varied pelvic reconstructions of Sts 14 [22, 23, 25, 30–32] and Sts 65 [33]. In A.L. 288–1, Sts 14, and Sts 65, a transverse entry into the pelvic inlet illustrates a beginning to the modern human birth mechanism [33], while midplane and outlet rotations remain debatable [2, 3, 14, 15, 17, 22–25]. The 0.9 to 1.4 Ma female Homo erectus pelvis, BSN49/P27, has a more gynecoid-shaped birth canal, distinct from the platypelloid pelvic shapes of the previously discussed australopiths [34] (but see [35]). The more expanded birth canal has been interpreted as an adaptation for birthing larger brained neonates in the genus Homo, although the mechanism of birth (i.e. rotational) was not explicitly discussed [34]. Reconstructions of the female Neandertal Tabun 1 pelvis show an expanded mediolateral dimension of the pelvic inlet and midplane combined with an expanded anterior-posterior outlet [36, 37]. These pelvic dimensions, as well as an increased neonatal cranial capacity in Neandertals, has led some researchers to infer a modern human-like rotational birth in this population [36, 38] while others have suggested a more primitive non-rotational transverse mechanism of delivery in their pelvic reconstruction [37]. Both interpretations are included in our comparison of these reconstructions to the A. sediba material. This paper expands upon the female hominin pelvic sample to include Australopithecus sediba [39]. Dated to 1.977 million years old [40], the two partial skeletons of an adult female and juvenile male include pelvic material that combines australopith and early Homo-like anatomies in a small-brained species [41, 42]. Unlike the platypelloid pelves of A. afarensis and A. africanus, the A. sediba pelvis is more anterior-posteriorly expanded, like the pelves of H. erectus and modern humans, albeit to a lesser degree [42]. Kibii et al. [42] proposed that the presence of Homo-like features in a small-brained hominin implied that pelvic adaptations may be related to locomotion rather than to birth constraints. Testing this hypothesis necessitates a characterization of birth in A. sediba. Furthermore, even if pelvic changes are driven by locomotion, they may still impact the mechanism of delivery, as evidenced by the interplay between locomotion and parturition in early australopiths [17]. Here, we reconstruct the birth canal of the A. sediba female (MH2) and characterize the birth process based on a composite pelvis reconstruction and estimated neonatal cranial and shoulder dimensions.

Discussion The discovery of female hominin pelvic remains helps to inform how the complex mechanism of human birth evolved. Chimpanzees, our closest living relatives, have relatively easy births. Small neonatal head size combined with a more spacious and uniformly shaped birth canal makes birth a rapid and relatively easy event that does not benefit from birth assistance. Humans, however, pair an enlarged neonatal cranial capacity with a birth canal that changes dimensions, resulting in fetal rotation in the birth canal. However, when rotational birth arose in human evolution remains unknown. Comparison of the birth mechanisms in fossil hominins has yielded varied results [15, 17, 23, 25, 30, 34, 37]. The composite pelvis achieved in this study allowed us to evaluate how birth may have occurred in A. sediba, a species that possesses a small cranial capacity, yet a more Homo-like pelvis with AP expansion of the birth canal. If A. sediba possessed obstetric challenges beyond that found in other australopiths, then perhaps these changes are related to obstetrics. This reconstruction of birth permits a test of the hypothesis that pelvic morphology in A. sediba was adapted for locomotion, rather than obstetrics [42]. The cranial dimensions and capacity for an A. sediba neonate were estimated using a regression-based analysis. With the LSQ regression equation, an estimated A. sediba neonatal brain volume of 162.1cc was predicted. The calculated cranial dimensions of biparietal breadth, fronto-occipital length, and brain height were then compared to the pelvic inlet, midplane, and outlet dimensions of the MH2 reconstruction to examine if rotational birth in A. sediba occurred. Our results indicate that a neonate of A. sediba would have had a transverse entry into the pelvic inlet, as has been suggested for other species of Australopithecus [17, 23, 26, 33]. The anterior-posterior dimension of the A. sediba pelvic inlet is too constrained to allow a frontal-occipital passage of a neonatal cranium, making a transverse or oblique entry the most likely option. After the transverse descent through the pelvic inlet, the fetal head would have room to continue transversely through the pelvic midplane. The MH1 ischium provides the most constricted dimensions due to the age and sex of the specimen. Although MH1 is a male specimen and therefore its use in an obstetrics analysis is unconventional, it is the only ischium assigned to A. sediba. The utilization of the MH1 ischium provides a minimum estimation of obstetric dimensions in MH2. However, even with these minimum dimensions (96.9mm), the fetal head length (89.2mm) would occupy 92.1% of the transverse dimension of the midplane, providing sufficient space for the fetal head to pass in a transverse orientation. If the fetal head and shoulder breadth can fit through these dimensions, it can be assumed that the neonate would also fit through the expanded dimensions a female ischium would afford. For midplane rotation to be necessary for the composite reconstructions in this study, the A. sediba neonatal brain size would need to increase 28.2–42.6% beyond the estimated 162.1cc. Back calculating from the LSQ regression equation, such an increase would predict an adult A. sediba brain volume of 572-664cc. This adult brain volume considerably exceeds the one known A. sediba brain volume (420cc) and is greater than any known australopith. As rotational movement by the fetus could result in a more difficult and complex birth, it is possible that fetal descent remained transversely oriented at the midplane. The pelvic outlet in A. sediba also does not exhibit bony obstruction relative to the neonatal cranial dimensions. The neonate would have had room to continue transversely, or obliquely out of the pelvic outlet. The transverse dimension of the outlet expands slightly to a length 7% longer than the estimated A. sediba neonatal cranium, not accounting for soft tissues. Any flexion of the neonate’s head would further decrease the diameter of the fetal head during the fetal exit of the birth canal under the pubic symphysis [3]. We have shown that this mechanism of birth—one predicted for A.L. 288–1 [17]—would increase the risk of shoulder dystocia in A. afarensis and is thus problematic [15]. In A.L. 288–1, the estimated neonatal shoulder breadth greatly exceeds the obstetric dimensions [15]. However, shoulder breadth would not have contributed to obstetric constraints with any pelvic dimensions in A. sediba. Even at their most constrained location (the AP pelvic inlet [80.8mm]), shoulder breadth (predicted to be 73.4 mm wide) could still pass unimpeded and may have been further reduced by cranially elevating the clavicles, “shrugging” to enter the birth canal [14]. The other pelvic planes had ample room for shoulder passage without the risk of dystocia. A similar birth mechanism has been suggested for other australopiths where the baby enters the pelvic inlet aligned transversely, but requires no further rotations [16, 17, 23, 25, 26] (but see [15, 30]) and is perhaps unsurprising given some of the primitive anatomies of A. sediba [42]. With the estimated neonatal cranial and maternal pelvic dimensions utilized in this study, non-rotational birth is possible in A. sediba. Nevertheless, the interspecific differences in fossil hominin pelvic morphology and fetal dimensions show that there is not a linear, gradual change from an “easy” birth to a “difficult” birth. Instead, the morphology of each specimen exhibits its own set of obstetric challenges. Hominin pelvic morphology is thought to be influenced by both locomotion [42] and obstetrics [34, 56]. The increase in encephalization throughout the hominin lineage has previously been thought to be the driving factor in expanding the AP dimensions of the pelvis (i.e. [34]). However, A. sediba possesses an AP expanded, Homo-like pelvis, with little evidence for obstetric constraints. This finding suggests that at least in A. sediba, the morphology of the pelvis was probably shaped by locomotion factors rather than solely obstetrics. Rotational birth The more gynecoid pelvis of early Homo may have been a result of obstetric requirements [34] and may have resulted in rotational birth [56]. However, A. sediba also possesses AP expansion in the pelvic midplane and raises the possibility of rotational birth in this taxon. To accommodate this interpretation, we describe fetal descent following determinations of Joulin’s Law which states that the neonate would rotate to coincide with the maximum dimension of the bony anatomy [18]. In the A. sediba pelvis, the maximum bony dimensions are not always in the transverse dimensions (Table 3). Therefore, following the assumption that the neonate would align to these maximum dimensions, a non-rotational birth pattern may not be the default for A. sediba. Following passage through the ML broad pelvic inlet, the midplane of A. sediba shows an anterior-posterior expansion to an even greater degree than other australopiths, making it more Homo-like. While the A. sediba neonate could pass through this plane transversely, there would be more space if it rotated and aligned the fronto-occipital length of the skull with the wider anteroposterior dimension of the maternal pelvis. Australopithecus midplane rotation has been proposed for A. africanus (i.e. Sts 14) by Berge et al. [23] and Berge and Goularas [30] who cite not only the increased AP expansion of the bony anatomy, but also uterine forces that will direct the neonate to rotate in this plane. As exhibited in Fig 3, the pelvic shape changes more dramatically from the inlet to the midplane in A. sediba than either the A. africanus or even H. erectus specimens. Instead, the shape change is more consistent with what is seen in Neandertals (Tabun 1) and modern humans. Additionally, this shape change is notable since A. africanus and A. sediba start at similar inlet indices. The final component to a difficult modern human birth is the fact that rigid shoulders cannot pass through the changing shape of the birth canal without some rotation [2, 3, 14]. Using the estimated neonatal shoulder breadth, the shoulders would not contribute to obstetrical obstruction in A. sediba in either a transverse or rotational birth scenario. We caution that our results are contingent on our reconstruction of the MH2 pelvis. As mentioned previously, the tenuous contact between the ilium and the sacrum in addition to the use of the MH1 ischium introduce the potential for error. We therefore anticipate that the findings presented here will be revisited should new pelvic fossils of A. sediba be found or should another team reconstruct the available material in a manner morphologically distinct from that presented here and elsewhere [42, 47].

Conclusion Reconstructing the pelvis of a female Australopithecus sediba (MH2) provides an assessment of the birth process in this Early Pleistocene hominin species. At the pelvic inlet, the neonatal head aligned with the maximum dimension of the pelvic inlet to enter the birth canal transversely. Lack of bony impingement into the birth canal, combined with a small neonatal head size would not necessitate further rotation of the fetus as it descended through the canal, though AP expansion of the maternal pelvis still indicates that rotational birth may have occurred. It is possible, even, that there was considerable variation in the birth mechanism in early australopiths, with varying amounts of neonatal rotation. Interestingly, the shape of the obstetric planes in A. sediba align more closely with the genus Homo than with the other australopiths. These findings imply that the anteroposterior expansion of the birth canal can occur without neonatal brain expansion in early hominins.

Supporting information S1 Table. This table shows all the data used for this study. BP: neonatal cranium biparietal breadth FO: frontal-occipital length of neonate cranium. AP: anterior-posterior dimension of maternal pelvis or composite pelvis ML: transverse dimension of maternal pelvis or composite pelvis. https://doi.org/10.1371/journal.pone.0221871.s001 (DOCX)

Acknowledgments Thank you to the Evolutionary Studies Institute and the University of the Witwatersrand Fossil Access Committee for permission to study original fossil material housed at the ESI in Johannesburg, South Africa. We are particularly grateful to L. Berger and B. Zipfel for making the Malapa fossils accessible. Thank you to H. Kurki for permission to use unpublished data. We thank M. Cartmill, S. Churchill, J. Kibii, S. Williams, J. Eyre, A. Claxton, M. Sobel, and C. Oreglia for helpful conversations about pelvis evolution, and reconstruction software. Finally, we thank three anonymous reviewers for their helpful comments and suggestions.