Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Sex differences in the pelvis did not evolve de novo in modern humans

Abstract

It is commonly assumed that the strong sexual dimorphism of the human pelvis evolved for delivering the relatively large human foetuses. Here we compare pelvic sex differences across modern humans and chimpanzees using a comprehensive geometric morphometric approach. Even though the magnitude of sex differences in pelvis shape was two times larger in humans than in chimpanzees, we found that the pattern is almost identical in the two species. We conclude that this pattern of pelvic sex differences did not evolve de novo in modern humans and must have been present in the common ancestor of humans and chimpanzees, and thus also in the extinct Homo species. We further suggest that this shared pattern was already present in early mammals and propose a hypothesis of facilitated variation as an explanation: the conserved mammalian endocrine system strongly constrains the evolution of the pattern of pelvic differences but enables rapid evolutionary change of the magnitude of sexual dimorphism, which in turn facilitated the rapid increase in hominin brain size.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Landmarks and semilandmarks.
Fig. 2: Joint PCA of pelvis shape for humans and chimpanzees.
Fig. 3: Sex differences in pelvis shape for humans (top row) and chimpanzees (bottom row).
Fig. 4: A comparison of pelvic sex differences in humans and chimpanzees independent of the species differences.
Fig. 5: Sex differences in the pelvic inlet in humans and chimpanzees.

Data availability

The data that support the findings of this study are openly available in an OSF repository80, https://osf.io/bd4gw/.

Code availability

The code written to analyse the data is openly available in an OSF repository80, https://osf.io/bd4gw/.

References

  1. 1.

    Fischer, B. & Mitteroecker, P. Covariation between human pelvis shape, stature, and head size alleviates the obstetric dilemma. Proc. Natl Acad. Sci. USA 112, 5655–5660 (2015).

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Fischer, B. & Mitteroecker, P. Allometry and sexual dimorphism in the human pelvis. Anat. Rec. 300, 698–705 (2017).

    Article  Google Scholar 

  3. 3.

    Huseynov, A. et al. Developmental evidence for obstetric adaptation of the human female pelvis. Proc. Natl Acad. Sci. USA 113, 5227–5232 (2016).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Schultz, A. H. Sex differences in the pelves of primates. Am. J. Phys. Anthropol. 7, 401–424 (1949).

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Tague, R. G. Sexual dimorphism in the human bony pelvis, with a consideration of the Neandertal pelvis from Kebara cave, Israel. Am. J. Phys. Anthropol. 88, 1–21 (1992).

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Washburn, S. L. Sex differences in the pubic bone. Am. J. Phys. Anthropol. 6, 199–208 (1948).

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Rogers, T. & Saunders, S. Accuracy of sex determination using morphological traits of the human pelvis. J. Forensic Sci. 39, 1047–1056 (1994).

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Hager, L. D. Sex differences in the sciatic notch of great apes and modern humans. Am. J. Phys. Anthropol. 99, 287–300 (1996).

    CAS  PubMed  Article  Google Scholar 

  9. 9.

    Durić, M., Rakocević, Z. & Donić, D. The reliability of sex determination of skeletons from forensic context in the Balkans. Forensic Sci. Int. 147, 159–164 (2005).

    PubMed  Article  Google Scholar 

  10. 10.

    Dunsworth, H. M. Expanding the evolutionary explanations for sex differences in the human skeleton. Evol. Anthropol. 29, 108–116 (2020).

    PubMed  Article  Google Scholar 

  11. 11.

    Grunstra, N. D. S. et al. Humans as inverted bats: a comparative approach to the obstetric conundrum. Am. J. Hum. Biol. 31, e23227 (2019).

    PubMed Central  Article  Google Scholar 

  12. 12.

    Leutenegger, W. Functional aspects of pelvic morphology in simian primates. J. Hum. Evol. 3, 207–222 (1974).

    Article  Google Scholar 

  13. 13.

    Pavličev, M., Romero, R. & Mitteroecker, P. Evolution of the human pelvis and obstructed labor: new explanations of an old obstetrical dilemma. Am. J. Obstet. Gynecol. https://doi.org/10.1016/j.ajog.2019.06.043 (2019).

  14. 14.

    Rosenberg, K. R. The evolution of modern human childbirth. Am. J. Phys. Anthropol. 35, 89–124 (1992).

    Article  Google Scholar 

  15. 15.

    Wood, B. A. & Chamberlain, A. T. The primate pelvis: allometry or sexual dimorphism? J. Hum. Evol. 15, 257–263 (1986).

    Article  Google Scholar 

  16. 16.

    Betti, L. Sexual dimorphism in the size and shape of the os coxae and the effects of microevolutionary processes. Am. J. Phys. Anthropol. 153, 167–177 (2014).

    PubMed  Article  Google Scholar 

  17. 17.

    Steudel, K. Sexual dimorphism and allometry in primate ossa coxae. Am. J. Phys. Anthropol. 55, 209–215 (1981).

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Tague, R. G. Big-bodied males help us recognize that females have big pelves. Am. J. Phys. Anthropol. 127, 392–405 (2005).

    PubMed  Article  Google Scholar 

  19. 19.

    Ridley, M. Pelvic sexual dimorphism and relative neonatal brain size really are related. Am. J. Phys. Anthropol. 97, 197–200 (1995).

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Moffett, E. A. Dimorphism in the size and shape of the birth canal across anthropoid primates. Anat. Rec. 300, 870–889 (2017).

    Article  Google Scholar 

  21. 21.

    Tague, R. G. Pelvic sexual dimorphism in a metatherian, Didelphis virginiana: implications for eutherians. J. Mammal. 84, 1464–1473 (2003).

    Article  Google Scholar 

  22. 22.

    Lovejoy, C. O. Evolution of human walking. Sci. Am. 259, 118–125 (1988).

    CAS  PubMed  Article  Google Scholar 

  23. 23.

    Gruss, L. T. & Schmitt, D. The evolution of the human pelvis: changing adaptations to bipedalism, obstetrics and thermoregulation. Philos. Trans R. Soc. Lond. B 370, 20140063 (2015).

    Article  Google Scholar 

  24. 24.

    Churchill, S. E. & Vansickle, C. Pelvic morphology in Homo erectus and early Homo. Anat. Rec. 300, 964–977 (2017).

    Article  Google Scholar 

  25. 25.

    Tague, R. G. & Lovejoy, C. O. The obstetric pelvis of A.L. 288-1 (Lucy). J. Hum. Evol. 15, 237–255 (1986).

    Article  Google Scholar 

  26. 26.

    Häusler, M. & Schmid, P. Comparison of the pelves of Sts 14 and AL 288-1: implications for birth and sexual dimorphism in australopithecines. J. Hum. Evol. 29, 363–383 (1995).

    Article  Google Scholar 

  27. 27.

    Tague, R. G. & Lovejoy, C. O. AL 288-1—Lucy or Lucifer: gender confusion in the Pliocene. J. Hum. Evol. 35, 75–94 (1998).

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Arsuaga, J. L. & Carretero, J. M. Multivariate analysis of the sexual dimorphism of the hip bone in a modern human population and in early hominids. Am. J. Phys. Anthropol. 93, 241–257 (1994).

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Kurki, H. K. Skeletal variability in the pelvis and limb skeleton of humans: does stabilizing selection limit female pelvic variation? Am. J. Hum. Biol. 25, 795–802 (2013).

    PubMed  Article  Google Scholar 

  30. 30.

    Torres‐Tamayo, N. et al. The torso integration hypothesis revisited in Homo sapiens: contributions to the understanding of hominin body shape evolution. Am. J. Phys. Anthropol. 167, 777–790 (2018).

    PubMed  Article  Google Scholar 

  31. 31.

    Torres‐Tamayo, N. et al. Assessing thoraco-pelvic covariation in Homo sapiens and Pan troglodytes: a 3D geometric morphometric approach. Am. J. Phys. Anthropol. 173, 514–534 (2020).

    PubMed  Article  Google Scholar 

  32. 32.

    Hirata, S., Fuwa, K., Sugama, K., Kusunoki, K. & Takeshita, H. Mechanism of birth in chimpanzees: humans are not unique among primates. Biol. Lett. 7, 686–688 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Nissen, H. W. & Yerkes, R. M. Reproduction in the chimpanzee: report on forty-nine births. Anat. Rec. 86, 567–578 (1943).

    Article  Google Scholar 

  34. 34.

    Huseynov, A., Ponce de León, M. S. & Zollikofer, C. P. E. Development of modular organization in the chimpanzee pelvis. Anat. Rec. 300, 675–686 (2017).

    Article  Google Scholar 

  35. 35.

    Rosenberg, K. & Trevathan, W. Bipedalism and human birth: the obstetrical dilemma revisited. Evol. Anthropol. 4, 161–168 (1995).

    Article  Google Scholar 

  36. 36.

    Wells, J. C. K. Between Scylla and Charybdis: renegotiating resolution of the ‘obstetric dilemma’ in response to ecological change. Philos. Trans R. Soc. Lond. B 370, 20140067 (2015).

    Article  Google Scholar 

  37. 37.

    Mitteroecker, P. & Fischer, B. Adult pelvic shape change is an evolutionary side effect. Proc. Natl Acad. Sci. USA 113, E3596 (2016).

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Mitteroecker, P. How human bodies are evolving in modern societies. Nat. Ecol. Evol. 3, 324–326 (2019).

    PubMed  Article  Google Scholar 

  39. 39.

    Zollikofer, C. P. E., Scherrer, M. & Ponce de León, M. S. Development of pelvic sexual dimorphism in hylobatids: testing the obstetric constraints hypothesis. Anat. Rec. 300, 859–869 (2017).

    Article  Google Scholar 

  40. 40.

    Calder, W. A. III The kiwi and egg design: evolution as a package deal. BioScience 29, 461–467 (1979).

    Article  Google Scholar 

  41. 41.

    Congdon, J. D. & Gibbons, J. W. Morphological constraint on egg size: a challenge to optimal egg size theory? Proc. Natl Acad. Sci. USA 84, 4145–4147 (1987).

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Cordero, G. A. Is the pelvis sexually dimorphic in turtles? Anat. Rec. 301, 1382–1389 (2018).

    Article  Google Scholar 

  43. 43.

    Lister, A. M. in The Proboscidea: Trends in Evolution and Paleoecology (eds Shoshani, J. & Tassy, P.) 254–259 (Oxford Univ. Press, 1996).

  44. 44.

    Schutz, H., Donovan, E. R. & Hayes, J. P. Effects of parity on pelvic size and shape dimorphism in Mus. J. Morphol. 270, 834–842 (2009).

    PubMed  Article  Google Scholar 

  45. 45.

    Tague, R. G. Pelvic sexual dimorphism among species monomorphic in body size: relationship to relative newborn body mass. J. Mammal. 97, 503–517 (2016).

    PubMed  Article  Google Scholar 

  46. 46.

    Crelin, E. S. & Newton, E. V. The pelvis of the free-tailed bat: sexual dimorphism and pregnancy changes. Anat. Rec. 164, 349–357 (1969).

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Nwoha, P. U. Sex differences in the bony pelvis of the fruit-eating bat, Eidolon helvum. Folia Morphol. 59, 291–295 (2000).

    CAS  Google Scholar 

  48. 48.

    Duetsch, J. & Peterson, R. Using pelvis morphology to identify sex in moose skeletal remains. Alces 48, 1–6 (2012).

    Google Scholar 

  49. 49.

    Kaufmann, C. A., Álvarez, M. C., L’Heureux, L. G. & Gutiérrez, M. A. Dimorfismo sexual en la pelvis de Lama guanicoe (Artiodactyla, Camelidae): un caso de aplicación en el sitio Paso Otero 1, Buenos Aires, Argentina. Mastozool. Neotrop. 20, 47–59 (2013).

  50. 50.

    West, B. A tale of two innominates. Circaea 6, 107–114 (1990).

    Google Scholar 

  51. 51.

    Berdnikovs, S. Evolution of sexual dimorphism in mustelids. PhD dissertation, Univ. Cincinnati (2005).

  52. 52.

    Schutz, H. Mammalian pelvic size and shape dimorphism: the effects of locomotion and parturition. PhD dissertation, Univ. Colorado at Boulder (2008).

  53. 53.

    Long, D. R. & Rose, F. L. Pelvic girdle size relationships in three turtle species. J. Herpetol. 23, 315–318 (1989).

    Article  Google Scholar 

  54. 54.

    Prieto-Marquez, A., Gignac, P. M. & Joshi, S. Neontological evaluation of pelvic skeletal attributes purported to reflect sex in extinct non-avian archosaurs. J. Vertebr. Paleontol. 27, 603–609 (2007).

    Article  Google Scholar 

  55. 55.

    Shatkovska, O. V., Ghazali, M., Mytiai, I. S. & Druz, N. Size and shape correlation of birds’ pelvis and egg: impact of developmental mode, habitat, and phylogeny. J. Morphol. 279, 1590–1602 (2018).

    PubMed  Article  Google Scholar 

  56. 56.

    Iguchi, T., Irisawa, S., Fukazawa, Y., Uesugi, Y. & Takasugi, N. Morphometric analysis of the development of sexual dimorphism of the mouse pelvis. Anat. Rec. 224, 490–494 (1989).

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Uesugi, Y., Taguchi, O., Noumura, T. & Iguchi, T. Effects of sex steroids on the development of sexual dimorphism in mouse innominate bone. Anat. Rec. 234, 541–548 (1992).

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    Steinetz, B. G. et al. Transmission of relaxin and estrogens to suckling canine pups via milk and possible association with hip joint laxity. Am. J. Vet. Res. 69, 59–67 (2008).

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Dehghan, F. et al. The effect of relaxin on the musculoskeletal system. Scand. J. Med. Sci. Sports 24, e220–e229 (2014).

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Middleton, E. R. Ecogeographic influences on trunk modularity in recent humans. PhD dissertation, New York Univ. (2015).

  61. 61.

    DeSilva, J. M. & Lesnik, J. J. Brain size at birth throughout human evolution: a new method for estimating neonatal brain size in hominins. J. Hum. Evol. 55, 1064–1074 (2008).

    PubMed  Article  Google Scholar 

  62. 62.

    Hublin, J.-J., Neubauer, S. & Gunz, P. Brain ontogeny and life history in Pleistocene hominins. Philos. Trans R. Soc. Lond. B. 370, 20140062 (2015).

    Article  Google Scholar 

  63. 63.

    Gerhart, J. & Kirschner, M. The theory of facilitated variation. Proc. Natl Acad. Sci. USA 104, 8582–8589 (2007).

    CAS  PubMed  Article  Google Scholar 

  64. 64.

    Pigliucci, M. & Muller, G. (eds) Evolution, the Extended Synthesis (MIT Press, 2010).

  65. 65.

    Laland, K. N. et al. The extended evolutionary synthesis: its structure, assumptions and predictions. Proc. R. Soc. Lond. B 282, 20151019 (2015).

    Google Scholar 

  66. 66.

    Adams, J., Greenwood, P. & Naylor, C. Evolutionary aspects of environmental sex determination. Int. J. Invertebr. Reprod. Dev. 11, 123–135 (1987).

    Article  Google Scholar 

  67. 67.

    Geffroy, B. & Douhard, M. The adaptive sex in stressful environments. Trends Ecol. Evol. 34, 628–640 (2019).

    PubMed  Article  Google Scholar 

  68. 68.

    Mittwoch, U. Sex-determining mechanisms in animals. Trends Ecol. Evol. 11, 63–67 (1996).

    CAS  PubMed  Article  Google Scholar 

  69. 69.

    Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  70. 70.

    DelPrete, H. Similarities in pelvic dimorphisms across populations. Am. J. Hum. Biol. 31, e23282 (2019).

    PubMed  Article  Google Scholar 

  71. 71.

    Gunz, P., Mitteroecker, P., Neubauer, S., Weber, G. W. & Bookstein, F. L. Principles for the virtual reconstruction of hominin crania. J. Hum. Evol. 57, 48–62 (2009).

    PubMed  Article  Google Scholar 

  72. 72.

    Reynolds, H. M., Snow, C. C. & Young, J. W. Spatial Geometry of the Human Pelvis Memo. Report No. FAA-AM-B2-9 (Federal Aviation Administration, 1982); https://www.faa.gov/data_research/research/med_humanfacs/oamtechreports/1980s/media/AM82-09.pdf

  73. 73.

    Fischer, B. & Mitteroecker, P. Data from: Covariation between human pelvis shape, stature, and head size alleviates the obstetric dilemma. Dryad https://doi.org/10.5061/DRYAD.2D728 (2016).

  74. 74.

    Gower, J. C. Generalized Procrustes analysis. Psychometrika 40, 33–51 (1975).

    Article  Google Scholar 

  75. 75.

    Rohlf, F. J. & Slice, D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Biol. 39, 40–59 (1990).

    Google Scholar 

  76. 76.

    Mitteroecker, P., Gunz, P., Windhager, S. & Schaefer, K. A brief review of shape, form, and allometry in geometric morphometrics, with applications to human facial morphology. Hystrix It. J. Mammal. 24, 59–66 (2013).

    Google Scholar 

  77. 77.

    Gunz, P., Mitteroecker, P. & Bookstein, F. L. in Modern Morphometrics in Physical Anthropology (ed. Slice, D.) 73–98 (Springer, 2005).

  78. 78.

    Gunz, P. & Mitteroecker, P. Semilandmarks: a method for quantifying curves and surfaces. Hystrix It. J. Mammal. 24, 103–109 (2013).

    Google Scholar 

  79. 79.

    Bookstein, F. L. Morphometric Tools for Landmark Data: Geometry and Biology (Cambridge Univ. Press, 1991).

  80. 80.

    Fischer, B., Grunstra N. D. S., Zaffarini, E. & Mitteroecker P. Data and code for ‘Sex differences in the pelvis did not evolve de novo in modern humans’. OSF https://doi.org/10.17605/OSF.IO/BD4GW (2021).

Download references

Acknowledgements

We thank the Center for Academic Research and Training in Anthropology, the Primate Research Institute of the University of Kyoto, F. Zachos (Mammal Collection, Natural History Museum Vienna), M. Häusler, C. Fornai and V. Krenn (University of Zurich and University of Vienna) for access to the chimpanzee pelves. We thank H. Reynolds for sharing the human landmark data. B.F. and P.M. acknowledge support from the Austrian Science Fund FWF (Elise Richter grant no. V-826 to B.F., grant no. P29397 to P.M.). N.D.S.G. was funded by a postdoctoral fellowship from the Konrad Lorenz Institute. E.Z. was supported by an Erasmus+ student exchange fellowship from the European Union.

Author information

Affiliations

Authors

Contributions

B.F. designed the comparative study. N.D.S.G., E.Z. and B.F. developed the chimpanzee landmark scheme and E.Z. and N.D.S.G. acquired the chimpanzee data. N.D.S.G. and B.F. derived the homologous landmark scheme. B.F. acquired the human data. B.F. and P.M. cleaned and analysed the data. B.F., N.D.S.G. and P.M. wrote the paper. All authors commented on the paper.

Corresponding author

Correspondence to Barbara Fischer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks Philipp Gunz, Nicole Torres and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Principal component analysis (PCA) of pelvis shape, jointly for humans and chimpanzees.

The black arrows represent the allometry vectors, which were estimated here using a non-pelvic size measure for each species (femoral head diameter in chimpanzees and body height in humans, compare Extended Data Fig. 2) in contrast to Fig. 2, where they were estimated based on pelvic centroid size. For these non-pelvic size variables, z-scores were computed independently for each species. The allometry vectors were then estimated by regressing the shape coordinates on the z-scores for each species and projected into the PC spaces. As in Fig. 2, the allometry vectors are species-specific but not sex-specific. The vectors are shown twice, superimposed on the sex means for each species. The direction of allometry is distinct from the direction of sex differences in both species. The individual data shown are the same as in Fig. 2. Each small point corresponds to an individual (humans: males=blue, females=red; chimpanzees: males=light blue, females=light red). The larger points in the same colors correspond to the sex means for each species.

Extended Data Fig. 2 Pelvic centroid size vs. femoral head diameter in chimpanzees and body height in humans, respectively.

Correlations for these pairs of size measures were 0.62 in chimpanzees and 0.70 in humans. Femoral head diameter was available for 31 out of 34 chimpanzees and stature was available for all 99 human individuals.

Extended Data Fig. 3 Inlet area in mm2 in humans and chimpanzees for females (red) and males (blue).

Inlet area was calculated as the area of the polygon defined by the 2D inlet landmarks. Humans: female mean=11540 (sd=1248), male mean=10376 (sd=1047); Chimpanzees: female mean=9517 (sd=1107), male mean=8661 (sd=1263).

Extended Data Fig. 4 Reanalysis of data from DelPrete (2019).

These data comprise means for females and males of 26 pelvic variables (linear distances, curved distances, and circumferences) from 6 populations (skeletal collections): White individuals from Hamann-Todd collection (HTW, 60 males, 59 females); Black individuals from Hamann-Todd (HTB, 60 m., 60 f.); Whites from Terry collection (TEW, 52 m., 52 f.), Blacks from Terry collection (TEB, 52 m., 52 f.); Coimbra collection (CO, 84 m., 71 f.); Spitalfields collection (SP, 31 m., 35 f.). We conducted a principal component analysis of these data. Shown are the sex means of males (blue) and females (red) for each population within the first three principal components (accounting for 94% of the total variance). The sex difference vectors (lines connecting the sex means) of the six populations are close to parallel in the first three principal components (panels A and B), illustrating the similar pattern of sex differences in the pelvis between human populations, despite some variation in magnitude (panel C). The magnitude was calculated as the Euclidean length of the sex differences vector.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fischer, B., Grunstra, N.D.S., Zaffarini, E. et al. Sex differences in the pelvis did not evolve de novo in modern humans. Nat Ecol Evol (2021). https://doi.org/10.1038/s41559-021-01425-z

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing