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Covariation of Fetal Skull and Maternal Pelvis During the Perinatal Period in Rhesus Macaques and Evolution of Childbirth in Primates

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Covariation of Fetal Skull and Maternal Pelvis During the Perinatal Period in Rhesus Macaques and Evolution of Childbirth in Primates Covariation of fetal skull and maternal pelvis during the perinatal period in rhesus macaques and evolution of childbirth in primates Mikaze Kawadaa,1, Masato Nakatsukasaa, Takeshi Nishimurab, Akihisa Kanekob, and Naoki Morimotoa,1 aLaboratory of Physical Anthropology, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan; and bPrimate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan Edited by Karen Rosenberg, University of Delaware, Newark, DE, and accepted by Editorial Board Member C. O. Lovejoy July 17, 2020 (received for review February 4, 2020) A large brain combined with an upright posture in humans has Given the relatively large head of the human neonate and the resulted in a high cephalopelvic proportion and frequently constrained pelvic width for efficient bipedalism, what could, obstructed labor. Fischer and Mitteroecker [B. Fischer, P. Mitteroecker, then, reduce the risk of obstructed labor? Do the morphologies Proc. Natl. Acad. Sci. U.S.A. 112, 5655−5660 (2015)] proposed that of the skull and pelvis covary and coevolve to reduce difficulty of the morphological covariations between the skull and pelvis childbirth? As the delivery process itself is primarily determined could have evolved to ameliorate obstructed labor in humans. by the interaction between the fetal head and maternal pelvis, The availability of quantitative data of such covariation, espe- the morphological covariation between the head and pelvis cially of the fetal skull and maternal pelvis, however, is still (cephalopelvic covariation [CPC]) has drawn considerable at- scarce. Here, we present direct evidence of morphological covari- tention. It has been reported that the sizes of the neonatal and ations between the skull and pelvis using actual mother−fetus Macaca mulatta maternal heads show a positive correlation in humans (27, 28). dyads during the perinatal period of ,aspecies Fischer and Mitteroecker (29) showed that humans with larger that exhibits cephalopelvic proportions comparable to modern heads tend to exhibit a rounder shape of the pelvic inlet with humans. We analyzed the covariation of the three-dimensional greater projection of the shorter sacrum to the dorsal direction morphology of the fetal skull and maternal pelvis using com- ANTHROPOLOGY puted tomography-based models. The covariation was mostly and the larger anteroposterior diameter in the pelvic outlet. observed at the pelvic locations related to the birth canal, and They also showed that such covariation between the head size the forms of the birth canal and fetal skull covary in such a way and pelvic shape is stronger in females than in males. Based on that reduces obstetric difficulties. Therefore, cephalopelvic co- these data, they proposed that the morphologies of the skull and variation could have evolved not only in humans, but also in pelvis covary to ease childbirth. other primate taxa in parallel, or it could have evolved already Small- to middle-sized primates (e.g., marmosets, squirrel in the early catarrhines. monkeys, macaques, and gibbons) also tend to exhibit high cephalopelvic proportions (7), since maternal body mass and skull | pelvis | obstetric dilemma | geometric morphometrics neonatal body and brain masses follow negative allometry (1, 30). In these taxa, the frequency of neonatal death during ncephalization and acquisition of bipedal locomotion are Ehallmarks of human evolution. In modern humans, adult and Significance neonatal brain volumes reach 1,400 and 400 cc on average, re- spectively (1–3). Bipedality with upright posture shaped the hu- Childbirth is frequently difficult for humans due to a cepha- man pelvis in a specific way compared to other primates. The locaudally short and dorsoventrally deep pelvis necessary for human pelvis is short and deep along the cephalocaudal and upright bipedality and a large neonatal brain. A tight fit be- dorsoventral directions, respectively, which is thought to be as- tween the neonatal head and maternal pelvic dimensions is, sociated with the stability and efficiency of bipedal locomotion however, found not only in humans, but also in some other (4–6). The human pelvic morphology results in a narrow birth primate taxa. The rhesus macaques show human-like cepha- canal, especially along the anteroposterior direction at the pelvic lopelvic proportions. We show that forms of the fetal skull and inlet (7–9). As a result of encephalization and adaptations for maternal pelvis during the perinatal period covary in ways to bipedalism, neonatal head and maternal pelvic dimensions typ- relax the obstructions of childbirth in rhesus macaques. This ically exhibit a tight fit in humans. The large human neonatal indicates that morphological covariation of the fetal skull and head relative to maternal pelvic sizes (a high cephalopelvic maternal pelvis could have evolved not only in humans, but proportion) frequently leads to difficulties in childbirth and has also in other primates in parallel, or it could be an example of a prompted a unique delivery process coupled with fetal rotation catarrhine synapomorphy. (refs. 7, 10–13, but see refs. 14, 15). In principle, the risks of obstructed labor should be reduced by Author contributions: N.M. designed research; M.K., M.N., T.N., A.K., and N.M. performed research; M.K. and N.M. contributed new reagents/analytic tools; M.K. and N.M. analyzed expanding true pelvic dimensions (4, 8, 9, 16, 17). There is a data; M.K., M.N., T.N., and N.M. wrote the paper; and M.K., T.N., A.K., and N.M. limitation in the capacity of pelvic expansion, however, since acquired data. increased pelvic width hampers energetic efficiency of bipedal The authors declare no competing interest. locomotion (refs. 8, 9, 16, 18, but see refs. 19, 20). Such a trade- This article is a PNAS Direct Submission. K.R. is a guest editor invited by the off that was hypothesized for the human pelvis is known as the Editorial Board. “obstetric dilemma” (7, 8, 18, 19, 21–25). This long-standing Published under the PNAS license. hypothesis was recently challenged by Warrener et al. (20), 1To whom correspondence may be addressed. Email: [email protected]. who showed that the broader pelves of females compared to jp or [email protected]. males do not result in energetic inefficiency. In either case, the This article contains supporting information online at https://www.pnas.org/lookup/suppl/ expansion of pelvic dimensions is limited, since a pelvic floor that doi:10.1073/pnas.2002112117/-/DCSupplemental. is too large could increase risk of visceral prolapse (26). First published August 17, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2002112117 PNAS | September 1, 2020 | vol. 117 | no. 35 | 21251–21257 Downloaded by guest on September 26, 2021 childbirth is relatively high (4, 10, 25). It is currently unknown between the fetal head and maternal pelvis (see also Materials whether the CPC evolved only in humans, in parallel in other and Methods). Second, we asked whether the fetal skull and primate taxa, or is a shared anthropoid synapomorphy. maternal pelvis show the covariation of three-dimensional mor- Addressing this question is of special relevance to infer the phologies (H0: hypothesis 0). If H0 is supported, we then asked evolutionary history of the CPC in primates. Here, we assess the whether the CPC corresponds to childbirth rather than to other CPC in Macaca, a genus that exhibits a high cephalopelvic pro- functions, such as locomotion (H1: hypothesis 1), and whether portion. The macaques exhibit a high cephalopelvic proportion the CPC reduces the obstruction of childbirth in rhesus comparable to humans (7, 31, 32), but do not exhibit obligate macaques (H2: hypothesis 2). To answer these questions, we bipedalism. Investigating the CPC in macaques could thus pro- assessed the three-dimensional morphologies of the fetal skull vide insights into the CPC hypothesis proposed by Fischer and and maternal pelvis using geometric morphometrics (Materials Mitteroecker (29). and Methods). While the CPC is the key for understanding the evolution of the delivery processes in primates, our current knowledge is Results limited in two aspects: First, direct data on the CPC are still In all of the mother−fetus dyads examined in this study, the scarce (but see ref. 15). Fischer and Mitteroecker (29) proposed anteroposterior diameter (see SI Appendix, Fig. S4 for defini- the hypothesis based on the within-individual covariation of the tion) of the fetal skull was considerably larger than the dorso- skull and pelvis in adults. However, the morphology of the ventral diameter of the pelvic outlet, and the fetal skull width neonatal head is determined not only by the maternal, but also was considerably larger than the mediolateral diameter of the by the paternal genetic factors. Thus, direct phenotypic data of pelvic outlet (SI Appendix, Table S2 and Figs S5 and S6 and the mother and its fetus are essential. Second, data on the co- Fig. 1). Specifically, the mediolateral diameter of the birth canal variation of the three-dimensional neonatal skull and maternal was smallest at the ischial spines (SI Appendix, Figs. S1, S4, S5, pelvic morphology remain unexplored. In this study, we investi- and S6). Thus, the major constraint of childbirth in rhesus ma- gate the CPC using direct data obtained from mother−fetus caques is the disproportion of the mediolateral diameters of both dyads of rhesus macaques (Macaca mulatta) (Fig. 1 and SI Ap- the fetal cranium and the pelvic outlet. The in silico simulation pendix, Figs. S1–S3 and Table S1). We obtained detailed skeletal showed that the space between the head and birth canal is larger morphological data derived from computed tomography (CT) when the fetal face is oriented toward the caudal direction than scans of perinatal rhesus macaques, such that the fetal skull when it is oriented toward the pubic direction of the mother in remained physically intact.
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