Evolutionary Biology

, Volume 39, Issue 1, pp 126–139 | Cite as

Evolvability of the Primate Pelvic Girdle

Research Article


The ilium and ischiopubic bones of the pelvis arise from different regulatory pathways, and as a result, they may be modular in their organization such that features on one bone may be morphologically integrated with each other, but not with features on the other pelvic bone. Modularity at this gross level of organization can act to increase the ability of these structures to respond to selection pressures (i.e., their evolvability). Furthermore, recent work has suggested that the evolution of the human pelvis was facilitated by low levels of integration and high levels of evolvability relative to other African apes. However, the extent of morphological integration and modularity of the bones of the pelvic girdle is not well understood, especially across the entire order of primates. Therefore, the hypothesis that the ilium and ischiopubis constitute separate modules was tested using three-dimensional landmark data that were collected from 752 pelves from 35 primate species. In addition, the hypothesis that the human pelvis demonstrates greatest evolvability was tested by comparing it to all other primates. The results demonstrate that regardless of phylogeny and locomotor function, the primate pelvis as a whole is characterized by low levels of overall integration and high levels of evolvability. In addition, the results support the developmental hypothesis of separate ilium and ischiopubis modular units. Finally, all primates, including humans, apparently share a common pattern of integration, modularity, and evolvability in the pelvis.


Integration Modularity Adaptation Bipedality Hominin Pelvis 



Thank you to the following osteological collections managers and staff for access to specimens in their care: D. Lunde and E. Westwig (American Museum of Natural History, NY), L. Gordon (National Museum of Natural History, Washington, D.C.), Y. Haile-Selassie and L. Jellema (Cleveland Museum of Natural History), J. Chupasko (Museum of Comparative Zoology, Harvard), W. Stanley (Field Museum of Natural History, Chicago), P. Jenkins and L. Tomsett (Natural History Museum, London), C. Lefèvre, J. Lesur-Gebremariam, J. Cuisin, and J. Villemain (Muséum national d’Histoire naturelle, Paris), and J. Youssouf and A. Randrianandrasana (Beza Mahafaly Osteological Collection, Madagascar). I thank Jeremiah Scott and Brian Villmoare for methodological discussions, Stephanie Meredith for providing the photographs in Fig. 1, and Natalie Cooper for assistance with R. Guilherme Garcia, Campbell Rolian, and Brian Villmoare kindly provided programs for tests on covariance matrices. Comments by Dan Lieberman, Brian Villmoare, and two anonymous reviewers significantly improved this manuscript. This study was supported by grants from NSF (DDIG, BCS-0752575), The Leakey Foundation, Sigma Xi, and Graduate and Professional Students Association and the School of Human Evolution and Social Change at Arizona State University.

Supplementary material

11692_2011_9143_MOESM1_ESM.xlsx (14 kb)
Supplementary material 1 (XLSX 14 kb)
11692_2011_9143_MOESM2_ESM.tif (146 kb)
Supplementary material 2 (TIFF 146 kb)
11692_2011_9143_MOESM3_ESM.xlsx (17 kb)
Supplementary material 3 (XLSX 16 kb)
11692_2011_9143_MOESM4_ESM.xlsx (17 kb)
Supplementary material 4 (XLSX 16 kb)


  1. Ackermann, R. R., & Cheverud, J. M. (2000). Phenotypic covariance structure in tamarins (genus Saguinus): A comparison of variation patterns using matrix correlation and common principal component analysis. American Journal of Physical Anthropology, 111, 489–501.PubMedGoogle Scholar
  2. Adair, F. (1918). The ossification centers of the fetal pelvis. The American Journal of Obstetrics and Diseases of Women and Children, 78, 175–199.Google Scholar
  3. Anemone, R. (1993). The functional anatomy of the hip and thigh in primates. In D. L. Gebo (Ed.), Postcranial adaptation in nonhuman primates (pp. 150–174). DeKalb, IL: Northern Illinois University Press.Google Scholar
  4. Arnold, C., Matthews, L. J., & Nunn, C. L. (2010). The 10kTrees website: A new online resource for primate phylogeny. Evolutionary Anthropology, 19, 114–118.Google Scholar
  5. Ashton, E. H., Flinn, R. M., Moore, W. J., Oxnard, C. E., & Spence, T. F. (1981). Further quantitative studies of form and function in the primate pelvis with special reference to Australopithecus. The Transactions of the Zoological Society of London, 36, 1–98.Google Scholar
  6. Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Review, 66, 101–157.Google Scholar
  7. Bastir, M., & Rosas, A. (2009). Mosaic evolution of the basicranium in Homo and its relation to modular development. Evolutionary Biology, 36, 57–70.Google Scholar
  8. Berger, L. R., de Ruiter, D. J., Churchill, S. E., Schmid, P., Carlson, K. J., Dirks, P. H. G. M., et al. (2010). Australopithecus sediba: A new species of Homo-like australopith from South Africa. Science, 328, 195–204.PubMedGoogle Scholar
  9. Blomberg, S. P., Garland, T., Jr., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57(4), 717–745.PubMedGoogle Scholar
  10. Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. New York: Cambridge University press.Google Scholar
  11. Bramble, D. M., & Lieberman, D. E. (2004). Endurance running and the evolution of Homo. Nature, 432, 345–352.PubMedGoogle Scholar
  12. Carrier, D. R., Chase, K., & Lark, K. G. (2005). Genetics of canid skeletal variation: Size and shape of the pelvis. Genome Research, 15(12), 1825–1830.PubMedGoogle Scholar
  13. Chevallier, A. (1977). Origine des ceintures scapulaires et pelviennes chez l’embryon d’oiseau. Journal of Embryology and Experimental Morphology, 42, 275–292.Google Scholar
  14. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36(3), 499–516.Google Scholar
  15. Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42(5), 958–968.Google Scholar
  16. Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145(1), 63–89.Google Scholar
  17. Cheverud, J. M. (1996a). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44–50.Google Scholar
  18. Cheverud, J. M. (1996b). Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. Journal of Evolutionary Biology, 9, 5–42.Google Scholar
  19. Cheverud, J. M., & Marroig, G. (2007). Comparing covariance matrices: Random skewers method compared to the common principal components model. Genetics and Molecular Biology, 30(2), 461–469.Google Scholar
  20. Cheverud, J. M., Wagner, G. P., & Dow, M. M. (1989). Methods for the comparative analysis of variation patterns. Systematic Zoology, 38(3), 201–213.Google Scholar
  21. Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. New York: Wiley.Google Scholar
  22. Escoufier, Y. (1973). Le traitement des variables vectorielles. Biometrics, 29, 751–760.Google Scholar
  23. Fleagle, J. G., & Anapol, F. C. (1992). The indriid ischium and the hominid hip. Journal of Human Evolution, 22, 285–305.Google Scholar
  24. Goswami, A. (2006a). Cranial modularity shifts during mammalian evolution. American Naturalist, 168(2), 270–280.PubMedGoogle Scholar
  25. Goswami, A. (2006b). Morphological integration in the carnivoran skull. Evolution, 60(1), 169–183.PubMedGoogle Scholar
  26. Goswami, A., & Polly, P. D. (2010). The influence of modularity on cranial morphological disparity in carnivora and primates (Mammalia). PLoS ONE, 5(3), e9517. doi: 10.1371/journal.pone.0009517.PubMedGoogle Scholar
  27. Grabowski, M. W., Polk, J. D., & Roseman, C. C. (2011). Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism. Evolution, 65(5), 1336–1356.PubMedGoogle Scholar
  28. Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36, 355–376.Google Scholar
  29. Hallgrímsson, B., & Lieberman, D. E. (2008). Mouse models and the evolutionary developmental biology of the skull. Integrative and Comparative Biology, 48(3), 373–384.PubMedGoogle Scholar
  30. Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. Yearbook of Physical Anthropology, 45, 131–158.Google Scholar
  31. Hansen, T. F., & Houle, D. (2004). Evolvability, stabilizing selection, and the problem of stasis. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 130–153). Cary, NC: Oxford University Press.Google Scholar
  32. Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219.PubMedGoogle Scholar
  33. Harmon, L. J., & Glor, R. E. (2010). Poor statistical performance of the mantel test in phylogenetic comparative analyses. Evolution, 64(7), 2173–2178.PubMedGoogle Scholar
  34. Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: Investigating evolutionary radiations. Bioinformatics, 24, 129–131.PubMedGoogle Scholar
  35. Jouffroy, F. K. (1975). Osteology and myology of the lemuriform postcranial skeleton. In I. Tattersall & R. W. Sussman (Eds.), Lemur biology (pp. 149–192). New York: Plenum Press.Google Scholar
  36. Jungers, W. L. (1976). Hindlimb and pelvic adaptations to vertical climbing and clinging in Megaladapis, a giant subfossil prosimian from Madagascar. Yearbook of Physical Anthropology, 20, 508–524.Google Scholar
  37. Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463–1464.PubMedGoogle Scholar
  38. Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution, and Systematics, 39, 115–132.Google Scholar
  39. Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11(4), 405–421.Google Scholar
  40. Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.PubMedGoogle Scholar
  41. Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution, 33, 402–416.Google Scholar
  42. Laurenson, R. D. (1964). The chondrification of the human ilium. The Anatomical Record, 148, 197–202.PubMedGoogle Scholar
  43. Lewton, K. L. (2010). Locomotor function and the evolution of the primate pelvis [Ph.D.]. Tempe: Arizona State University.Google Scholar
  44. Lleonart, J., Salat, J., & Torres, G. J. (2000). Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93.PubMedGoogle Scholar
  45. Lovejoy, C. O. (1975). Biomechanical perspectives on the lower limb of early hominids. In R. H. Tuttle (Ed.), Primate functional morphology and evolution (pp. 291–326). Chicago: Aldine.Google Scholar
  46. Lovejoy, C. O., Suwa, G., Spurlock, L., Asfaw, B., & White, T. D. (2009). The pelvis and femur of Ardipithecus ramidus: The emergence of upright walking. Science, 326(5949), 71–77.Google Scholar
  47. MacLatchy, L. (1998). Reconstruction of hip joint function in extant and extinct fossil primates. In E. Strasser, J. G. Fleagle, A. Rosenberger, & H. M. McHenry (Eds.), Primate locomotion: Recent advances (pp. 111–130). New York: Plenum Press.Google Scholar
  48. Malashichev, Y., Borkhvardt, V., Christ, B., & Scaal, M. (2005). Differential regulation of avian pelvic girdle development by the limb field ectoderm. Anatomy and Embryology, 210, 187–197.PubMedGoogle Scholar
  49. Malashichev, Y., Christ, B., & Prols, F. (2008). Avian pelvis originates from lateral plate mesoderm and its development requires signals from both ectoderm and paraxial mesoderm. Cell and Tissue Research, 331, 595–604.PubMedGoogle Scholar
  50. Manly, B. F. J. (1997). Randomization, bootstrap and Monte Carlo methods in biology. Boca Raton, FL: CRC Press.Google Scholar
  51. Marroig, G., & Cheverud, J. M. (2001). A comparison of phenotypuc variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys. Evolution, 55, 2576–2600.PubMedGoogle Scholar
  52. Marroig, G., & Cheverud, J. M. (2004a). Cranial evolution in sakis (Pithecia, Platyrrhini) I: Interspecific differentiation and allometric patterns. American Journal of Physical Anthropology, 125, 266–278.PubMedGoogle Scholar
  53. Marroig, G., & Cheverud, J. M. (2004b). Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? American Naturalist, 163(3), 417–428.PubMedGoogle Scholar
  54. Marroig, G., Shirai, L. T., Porto, A., de Oliveira, F. B., & De Conto, V. (2009). The evolution of modularity in the mammalian skull II: Evolutionary consequences. Evolutionary Biology, 36, 136–148.Google Scholar
  55. McNulty, K. P. (2005). A geometric morphometric assessment of the hominoid supraorbital region: Affinities of the Eurasian Miocene hominoids Dryopithecus, Graecopithecus, and Sivapithecus. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 349–373). New York: Kluwer.Google Scholar
  56. Mitteroecker, P., & Bookstein, F. (2008). The evolutionary role of modularity and integration in the hominoid cranium. Evolution, 62(4), 943–958.PubMedGoogle Scholar
  57. Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.Google Scholar
  58. O’Rahilly, R., & Gardner, E. (1975). The timing and sequence of events in the development of the limbs in the human embryo. Anatomy and Embryology, 148, 1–23.PubMedGoogle Scholar
  59. Pavlicev, M., Cheverud, J. M., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157–170.Google Scholar
  60. Pellegrini, M., Pantano, S., Fumi, M. P., Lucchini, F., & Forabosco, A. (2001). Agenesis of the scapula in Emx2 homozygous mutants. Developmental Biology, 232, 149–156.PubMedGoogle Scholar
  61. Pomikal, C., Blumer, R., & Streicher, J. (2011). Four-dimensional analysis of early pelvic girdle development in Rana temporaria. Journal of Morphology, 272, 287–301.PubMedGoogle Scholar
  62. Pomikal, C., & Streicher, J. (2010). 4D-analysis of early pelvic girdle development in the mouse (Mus musculus). Journal of Morphology, 271(1), 116–126.PubMedGoogle Scholar
  63. Porto, A., de Oliveira, F. B., Shirai, L. T., de Conto, V., & Marroig, G. (2009). The evolution of modularity in the mammalian skull I: Morphological integration patterns and magnitudes. Evolutionary Biology, 36, 118–135.Google Scholar
  64. R Development Core Team. (2011). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  65. Revell, L. (2007). Skewers: A program for Cheverud’s random skewers method of matrix comparison. http://anolis.oeb.harvard.edu/~liam/programs/.
  66. Riedl, R. (1977). A systems-analytical approach to macro-evolutionary phenomena. The Quarterly Review of Biology, 52, 351–370.PubMedGoogle Scholar
  67. Robinson, J. T. (1972). Early hominid posture and locomotion. Chicago: The University of Chicago Press.Google Scholar
  68. Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39(1), 40–59.Google Scholar
  69. Rolian, C. (2009). Integration and evolvability in primate hands and feet. Evolutionary Biology, 36(1), 100–117.Google Scholar
  70. Scott, J. E. (2010). Nonsocial influences on canine size in anthropoid primates [Ph.D.]. Tempe: Arizona State University.Google Scholar
  71. Sigmon, B. A., & Farslow, D. L. (1986). The primate hindlimb. In D. R. Swindler & J. Erwin (Eds.), Comparative primate biology, volume 1: Systematics, evolution, and anatomy (pp. 671–718). New York: Alan R. Liss, Inc.Google Scholar
  72. Steppan, S. J. (2004). Phylogenetic comparisons of multivariate data. In M. Piglicucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 325–344). New York: Oxford University Press.Google Scholar
  73. Stern, J. T., & Susman, R. L. (1983). The locomotor anatomy of Australopithecus afarensis. American Journal of Physical Anthropology, 60, 279–312.PubMedGoogle Scholar
  74. Strait, D. S. (2001). Integration, phylogeny, and the hominid cranial base. American Journal of Physical Anthropology, 114, 273–297.PubMedGoogle Scholar
  75. Tague, R. G. (2005). Big-bodied males help us recognize that females have big pelves. American Journal of Physical Anthropology, 127, 392–405.PubMedGoogle Scholar
  76. Villmoare, B., Fish, J., & Jungers, W. (2011). Selection, morphological integration, and strepsirrhine locomotor adaptations. Evolutionary Biology, 38(1), 88–99.Google Scholar
  77. Wagner, G. P. (1984). On the eigenvalue distribution of genetic and phenotypic dispersion matrices: Evidence for a nonrandom organization of quantitative character variation. Journal of Mathematical Biology, 21, 77–95.Google Scholar
  78. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36(1), 36–43.Google Scholar
  79. Williams, S. A. (2010). Morphological integration and the evolution of knuckle-walking. Journal of Human Evolution, 58, 432–440.PubMedGoogle Scholar
  80. Willis, J. H., Coyne, J. A., & Kirkpatrick, M. (1991). Can one predict the evolution of quantitative characters without genetics? Evolution, 45, 441–444.Google Scholar
  81. Young, N. M. (2006). Function, ontogeny and canalization of shape variance in the primate scapula. Journal of Anatomy, 209, 623–636.PubMedGoogle Scholar
  82. Young, N. M., & Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59, 2691–2704.PubMedGoogle Scholar
  83. Young, N. M., Wagner, G. P., & Hallgrímsson, B. (2010). Development and the evolvability of human limbs. Proceedings of the National Academy of Science, 107, 3400–3405.Google Scholar
  84. Zelditch, M. L., Wood, A. R., & Swiderski, D. L. (2009). Building developmental integration into functional systems: Function-induced integration of mandibular shape. Evolutionary Biology, 36, 71–87.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Human Evolutionary BiologyHarvard UniversityCambridgeUSA

Personalised recommendations