A large brain combined with an upright posture in humans has resulted in a high cephalopelvic proportion and frequently obstructed labor. Fischer and Mitteroecker [B. Fischer, P. Mitteroecker, Proc. Natl. Acad. Sci. U.S.A. 112, 5655−5660 (2015)] proposed that the morphological covariations between the skull and pelvis could have evolved to ameliorate obstructed labor in humans. The availability of quantitative data of such covariation, especially of the fetal skull and maternal pelvis, however, is still scarce. Here, we present direct evidence of morphological covariations between the skull and pelvis using actual mother−fetus dyads during the perinatal period of Macaca mulatta, a species that exhibits cephalopelvic proportions comparable to modern humans. We analyzed the covariation of the three-dimensional morphology of the fetal skull and maternal pelvis using computed tomography-based models. The covariation was mostly observed at the pelvic locations related to the birth canal, and the forms of the birth canal and fetal skull covary in such a way that reduces obstetric difficulties. Therefore, cephalopelvic covariation could have evolved not only in humans, but also in other primate taxa in parallel, or it could have evolved already in the early catarrhines.

Significance During human birth, the risk of complications is relatively high because of the comparatively large dimensions of the fetal head and shoulders relative to the maternal birth canal. Here we show that humans exhibit a developmental mode of the shoulders that likely contributes to mitigating obstetrical problems. Human shoulder growth is decelerated before birth but accelerated after birth, which stands in contrast to the more uniform shoulder growth trajectories of chimpanzees and macaques. This indicates that fetal developmental modifications were required during human evolution not only in the head but also in the shoulders to compensate obstetrical constraints.

Pelvic morphology exhibits a particular sexual dimorphism in humans, which reflects obstetrical constraints due to the tight fit between neonates and mothers. Huseynov et al. [ Proc. Natl. Acad. Sci. U.S.A. 113 , 5227–5232 (2016)] showed that in humans, pelvic sexual dimorphism is greatest around the age of highest fertility, and it becomes less marked in association with menopause in females. They proposed that this reflects changes of obstetrical versus locomotor functional demands in females. It remains unknown whether such developmental adjustment of the pelvic morphology is unique to humans. Macaques exhibit human-like cephalopelvic proportions, but they lack menopause and usually maintain fertility throughout adulthood. Here, we track pelvic development in Japanese macaques from neonate to advanced ages using computed tomography-based data. We show that female pelvic morphology changes throughout adult life, reaching the obstetrically most favorable shape at advanced ages rather than around primiparity. We hypothesize that pelvic morphology in Japanese macaques is developmentally adjusted to childbirth at advanced ages, where obstetrical risks are potentially higher than at younger ages. Our data contribute to the growing evidence that the female primate pelvis changes its morphology during the whole lifespan, possibly adjusting for changing functional demands during adulthood.