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Gradual exacerbation of obstetric constraints during hominoid evolution implied by re-evaluation of cephalopelvic fit in chimpanzees

Nature Ecology & Evolution (2024)Cite this article

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Abstract

Under the obstetrical dilemma hypothesis, sexual dimorphism in pelvic shape is a solution to accommodate high fetopelvic constraints. It is therefore unclear why chimpanzees display a human-like pattern of pelvic sexual dimorphism despite having easier births enabled by small neonates and capacious pelvic canals. Here we reassessed chimpanzee fetopelvic fit using three-dimensional simulations, revealing a similarly constricted midpelvis as in humans, with even narrower outlet dimensions. Geometric morphometric analyses confirm that female chimpanzees have larger pelvic canals than males despite a smaller body size and a morphology that maximizes pelvic dimensions favourable for parturition, particularly in smaller-bodied individuals. Together with evidence for increased neurological immaturity at birth relative to monkeys, our findings imply substantial obstetric constraints in chimpanzees and possibly other apes. We therefore propose that difficult birth did not arise abruptly in Homo with increasing encephalization but evolved gradually through a series of obstetric compromises from an already constricted birth canal shared across anthropoid primates. Specifically, we propose that obstetric selection pressures exacerbated incrementally with the stiffening of the symphysis that accompanied body size increase in hominoids, while subsequent adaptations to bipedalism shortened the ilium. The resulting contorted birth canal required obligatory fetal rotation, thus greatly increasing birth difficulty.

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Fig. 1: Cephalopelvic fit for chimpanzees versus modern humans.
Fig. 2: Quantification of the cephalopelvic fit in chimpanzees.
Fig. 3: Sexual dimorphism in pelvic shape in chimpanzees (n = 29, 16 females and 13 males).
Fig. 4: Female chimpanzee pelvic shape differences driven by size.
Fig. 5: Hominins and apes are neurologically more immature at birth than other primates.
Fig. 6: Adaptations leading to birth difficulty in humans over time.

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Data availability

The data supporting the manuscript are available in the Supplementary Information or via GitHub at https://github.com/NicoleWebb/Pan-Cephalopelvic-Fit-Paper.

Code availability

The source code for all analyses included in the paper are available via GitHub at https://github.com/NicoleWebb/Pan-Cephalopelvic-Fit-Paper.

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Acknowledgements

We thank K. Isler for discussion on neurological development and compiling the data on brain mass of newborn and adult anthropoid primates. We also extend our gratitude to F. Mazelis, G. Bravo Morante and N. Torres-Tamayo for their technical input. The following institutions provided curatorial assistance and access to their skeletal and digital collections: the Anthropological Institute and Museum, University of Zurich; the Natural History Museum, Vienna; the University of California, San Diego; the Zoological Museum, University of Zurich; the Natural History Museum, Basel; the KUPRI Digital Museum Collection; and the Smithsonian National Museum of Natural History, Washington. This work was funded by the Swiss National Science Foundation grant nos. 31003A_156299 (M.H.) and 31003A_176319 (M.H.) and is part of the Leibniz-Kooperative Exzellenz Project K438/2022 (N.M.W.).

Author information

Author notes

  1. These authors contributed equally: Nicole M. Webb, Martin Haeusler.

Authors and Affiliations

  1. Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt, Germany

    Nicole M. Webb & Laura M. Watson

  2. Institute of Evolutionary Medicine, University of Zurich, Zurich, Switzerland

    Nicole M. Webb, Cinzia Fornai, Viktoria A. Krenn & Martin Haeusler

  3. Department of Research in Occlusion Medicine, Vienna School of Interdisciplinary Dentistry—VieSID, Klosterneuburg, Austria

    Cinzia Fornai

  4. Center for Clinical Research, University Clinic of Dentistry Vienna, Medical University of Vienna, Vienna, Austria

    Cinzia Fornai

  5. Human Evolution and Archaeological Sciences, University of Vienna, Vienna, Austria

    Cinzia Fornai

  6. Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria

    Cinzia Fornai & Viktoria A. Krenn

  7. Fraunhofer Austria Innovation Center for Digitalization and Artificial Intelligence KI4LIFE, Klagenfurt, Austria

    Viktoria A. Krenn

  8. Institute for Archaeological Sciences, University of Tübingen, Tübingen, Germany

    Laura M. Watson

  9. Palaeontological Institute and Museum, University of Zurich, Zurich, Switzerland

    Eva C. Herbst

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Contributions

N.M.W., C.F. and M.H. conceived and designed the study. C.F., V.A.K., N.M.W. and M.H. collected data used in the analyses. N.M.W., C.F., E.C.H., V.A.K. and M.H. performed analyses. N.M.W., V.A.K., C.F. and M.H. prepared the figures and publication materials. N.M.W., C.F., V.A.K., E.C.H. and M.H. drafted the initial manuscript version. All authors discussed results/interpretations and edited subsequent versions of the manuscript, with L.M.W. contributing to later drafts.

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Correspondence to Nicole M. Webb, Cinzia Fornai or Martin Haeusler.

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Extended data

Extended Data Fig. 1 The birth canal of chimpanzees.

a, The birth canal can be approximated by a cylinder. The pelvic inlet represents an oblique cylinder section and since the inlet anteroposterior diameter I–I´ is not the smallest diameter of the cylinder it is not obstetrically relevant, in contrast to the pelvic midpelvis, whose anteroposterior diameter M–M´ is perpendicular to the longitudinal axis of the birth canal. When the fetus reaches the pelvic outlet O–O´, the tip of the sacrum together with the coccyx has to nutate backwards to enlarge the space of the bony birth canal. b, The fetal head in a fully extended position, which is the typical head orientation for monkeys. c, The fetal head in a fully flexed position, which is the usual head orientation for humans. Both head orientations occur in chimpanzees and are obstetrically equivalent. The neck is only schematically visualised.

Extended Data Fig. 2 Recreation of Schultz’s (1949) popular cephalopelvic fit diagram showing the differences between pelvic inlet dimensions and fetal head sizes across primates.

Note the ample space of the anteroposterior pelvic inlet diameters relative to the fetal head for the great apes which contrasts with that of humans in which the fetal head dimensions exceed that of the birth canal in these particular dimensions. Adapted with permission from ref. 6, John Wiley & Sons.

Extended Data Fig. 3 Landmark configuration in anterior (left) and posterior view (right) used in the 3D geometric morphometric analyses.

The 52 fixed landmarks are depicted in light blue and the 38 curve semilandmarks on six curves are in dark blue.

Extended Data Fig. 4 Thin-plate-spline warpings based on shape changes observed at the extremes of the first three PC axes.

From left to right: anterior, inferior and lateral views based on the complete landmark configuration (see the PCA of Fig. 3).

Extended Data Fig. 5 Phylogenetic reduced major axis regressions for Old and New World monkeys and apes.

The red line signifies the actual slope for the regression whereas the dashed grey line represents the null hypothesis for the relationship between the observed traits where the slope is set to the default of 1. All pRMA regressions assume a Brownian evolution model variance-covariance structure.

Supplementary information

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Supplementary Tables

Supplementary Table 1. Landmark descriptions included in 3DGM analyses; Table 2. Regression raw data and related sources; and Table 3. Results of phylogenetic regression analyses.

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Webb, N.M., Fornai, C., Krenn, V.A. et al. Gradual exacerbation of obstetric constraints during hominoid evolution implied by re-evaluation of cephalopelvic fit in chimpanzees. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02558-7

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