Human shoulder development is adapted to obstetrical constraints
Edited by Robert Tague, Louisiana State University, Baton Rouge, LA; received August 12, 2021; accepted March 2, 2022 by Editorial Board Member C. O. Lovejoy
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.
Abstract
In humans, obstetrical difficulties arise from the large head and broad shoulders of the neonate relative to the maternal birth canal. Various characteristics of human cranial development, such as the relatively small head of neonates compared with adults and the delayed fusion of the metopic suture, have been suggested to reflect developmental adaptations to obstetrical constraints. On the other hand, it remains unknown whether the shoulders of humans also exhibit developmental features reflecting obstetrical adaptation. Here we address this question by tracking the development of shoulder width from fetal to adult stages in humans, chimpanzees, and Japanese macaques. Compared with nonhuman primates, shoulder development in humans follows a different trajectory, exhibiting reduced growth relative to trunk length before birth and enhanced growth after birth. This indicates that the perinatal developmental characteristics of the shoulders likely evolved to ease obstetrical difficulties such as shoulder dystocia in humans.
Data Availability
All study data are included in the article and/or SI Appendix.
Acknowledgments
We thank the staff of the Center for Human Evolution Modeling Research at KUPRI for assistance in this study and daily care of the subjects. We thank P. Jans for help with CT scanning. We also appreciate the Great Ape Information Network project (https://shigen.nig.ac.jp/gain/about_gain.jsp) and Tennoji Zoo for their help in collecting great ape specimens. This research is an outcome of the strategic research partnership between Kyoto University and the University of Zurich. The insightful comments of the editor and two anonymous reviewers are greatly acknowledged. This study was supported by Cooperative Research Program at KUPRI Grants 2015-A-22, 2018-C-8, 2019-C-15, and 2020-B-26 and Japan Society for the Promotion of Science KAKENHI Grant Number 17K07585.
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Cover image: Pictured is an ocellated antbird (Phaenostictus mcleannani). Henry S. Pollock et al. analyzed mist net capture data for 57 Neotropical understory bird species in a relatively large, intact forest preserve in Panama to track population changes from 1977-2020. The authors found that 40 of the studied bird species experienced population declines, with 35 species experiencing severe declines to less than 50% of their initial abundances. The results corroborate previous findings that bird populations are declining globally and suggest that even birds in protected forests are experiencing declines. See the article by Pollock et al., e2108731119. Image credit: John Whitelaw (photographer).
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Copyright © 2022 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Data Availability
All study data are included in the article and/or SI Appendix.
Submission history
Received: August 12, 2021
Accepted: March 2, 2022
Published online: April 11, 2022
Published in issue: April 19, 2022
Keywords
Acknowledgments
We thank the staff of the Center for Human Evolution Modeling Research at KUPRI for assistance in this study and daily care of the subjects. We thank P. Jans for help with CT scanning. We also appreciate the Great Ape Information Network project (https://shigen.nig.ac.jp/gain/about_gain.jsp) and Tennoji Zoo for their help in collecting great ape specimens. This research is an outcome of the strategic research partnership between Kyoto University and the University of Zurich. The insightful comments of the editor and two anonymous reviewers are greatly acknowledged. This study was supported by Cooperative Research Program at KUPRI Grants 2015-A-22, 2018-C-8, 2019-C-15, and 2020-B-26 and Japan Society for the Promotion of Science KAKENHI Grant Number 17K07585.
Notes
This article is a PNAS Direct Submission. R.T. is a guest editor invited by the Editorial Board.
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The authors declare no competing interest.
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