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A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids

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Abstract

By comparing species-specific developmental patterns, we can approach the question of how development shapes adult morphology and contributes to the evolution of novel forms. Studies of evolutionary changes to brain development in primates can provide important clues about the emergence of human cognition, but are hindered by the lack of preserved neural tissue in the fossil record. As a proxy, we study the shape of endocasts, virtual imprints of the endocranial cavity, using 3D geometric morphometrics. We have previously demonstrated that the pattern of endocranial shape development is shared by modern humans, chimpanzees and Neanderthals after the first year of life until adulthood. However, whether this represents a common hominoid mode of development is unknown. Here, we present the first characterization and comparison of ontogenetic endocranial shape changes in a cross-sectional sample of modern humans, chimpanzees, gorillas, orangutans and gibbons. Using developmental simulations, we demonstrate that from late infancy to adulthood ontogenetic trajectories are similar among all hominoid species, but differ in the amount of shape change. Furthermore, we show that during early ontogeny gorillas undergo more pronounced shape changes along this shared trajectory than do chimpanzees, indicative of a dissociation of size and shape change. As shape differences between species are apparent in even our youngest samples, our results indicate that the ontogenetic trajectories of extant hominoids diverged at an earlier stage of ontogeny but subsequently converge following the eruption of the deciduous dentition.

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References

  • Ackermann, R., & Krovitz, G. E. (2002). Common patterns of facial ontogeny in the hominid lineage. The Anatomical Record, 269(3), 142–147.

  • Alberch, P., Gould, S. J., Oster, G. F., & Wake, D. B. (1979). Size and shape in ontogeny and phylogeny. Paleobiology, 5, 296–317.

  • Anemone, R. L., & Swindler, D. R. (1999). Heterochrony and sexual dimorphism in the skull of the Liberian chimpanzee (Pan troglodytes verus). International Journal of Anthropology, 14(1), 19–30.

    Google Scholar 

  • Ashton, E. H. (1957). Age changes in the basicranial axis of the Anthropoidea. In Proceedings of the Zoological Society of London (Vol. 129, No. 1, pp. 61–74). Blackwell Publishing Ltd.

  • Ashton, E. H., Moore, W. J., & Spence, T. F. (1976). Growth changes in endocranial capacity in the Cercopithecoidea and Hominoidea. Journal of Zoology, 180(3), 355–365.

    Google Scholar 

  • Ashton, E. H., & Spence, T. F. (1958). Age changes in the cranial capacity and foramen magnum of hominoids. In Proceedings of the Zoological Society of London (Vol. 130, No. 2, pp. 169–181). Blackwell Publishing Ltd.

  • Ashton, E. H., & Zuckerman, S. (1956). Age changes in the position of the foramen magnum in hominoids. In Proceedings of the Zoological Society of London (Vol. 126, No. 2, pp. 315–326). Blackwell Publishing Ltd.

  • Bastir, M., & Rosas, A. (2004). Facial heights: Evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. Journal of Human Evolution, 47(5), 359–381.

    PubMed  Google Scholar 

  • Bastir, M., & Rosas, A. (2009). Mosaic evolution of the basicranium in Homo and its relation to modular development. Evolutionary Biology, 36(1), 57–70.

    Google Scholar 

  • Bastir, M., Rosas, A., & O’Higgins, P. (2006). Craniofacial levels and the morphological maturation of the human skull. Journal of Anatomy, 209(5), 637–654.

    PubMed Central  PubMed  Google Scholar 

  • Bastir, M., Rosas, A., Stringer, C., Manuel Cuétara, J., Kruszynski, R., Weber, G. W., et al. (2010). Effects of brain and facial size on basicranial form in human and primate evolution. Journal of Human Evolution, 58(5), 424–431.

    PubMed  Google Scholar 

  • Berge, C., & Penin, X. (2004). Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis. American Journal of Physical Anthropology, 124(2), 124–138.

    PubMed  Google Scholar 

  • Biegert, J. (1957). Der Formwandel des Primatenschädels und seine Beziehungen zur ontogenetischen Entwicklung und den phylogenetischen Spezialisationen der Kopforgane. Gegenbaurs morphologisches Jahrbuch, 98, 77–199.

    Google Scholar 

  • Biegert, J. (1963). The evaluation of characteristics of the skull, hands and feet for primate taxonomy. In S. L. Washburn (Ed.), Classification and human evolution (pp. 116–145). London: Methuen & Co., Ltd.

    Google Scholar 

  • Bienvenu, T., Guy, F., Coudyzer, W., Gilissen, E., Roualdès, G., Vignaud, P., et al. (2011). Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts. American Journal of Physical Anthropology, 145(2), 231–246.

    PubMed  Google Scholar 

  • Bischoff, T. L. W. (1867). Über die Verschiedenheit in der Schädelbildung des Gorilla, Chimpansé und Orang-outang: Vorzüglich nach Geschlecht und Alter, Nebst Einer Bemerkung überdie Darwinsche Theorie. Verlag der K. Akademie, in commission bei G. Franz.

  • Björk, A. (1955). Cranial base development: A follow-up x-ray study of the individual variation in growth occurring between the ages of 12 and 20 years and its relation to brain case and face development. American Journal of Orthodontics, 41(3), 198–225.

    Google Scholar 

  • Blaney, S. P. A. (1986). An allometric study of the frontal sinus in Gorilla, Pan and Pongo. Folia Primatologica, 47(2–3), 81–96.

    CAS  Google Scholar 

  • Bolk, L. (1909). On the position and displacement of the foramen magnum in the Primates. Verhandelingen der Koninklijke Akademie van Wetenschappen, 12, 362–377.

    Google Scholar 

  • Bookstein, F. L. (1997). Landmark methods for forms without landmarks: Morphometrics of group differences in outline shape. Medical Image Analysis, 1(3), 225–243.

    CAS  PubMed  Google Scholar 

  • Breuer, T., Hockemba, M. B. N., Olejniczak, C., Parnell, R. J., & Stokes, E. J. (2009). Physical maturation, life-history classes and age estimates of free‐ranging western gorillas—insights from Mbeli Bai, Republic of Congo. American Journal of Primatology, 71(2), 106–119.

  • Bruner, E. (2004). Geometric morphometrics and paleoneurology: bRain shape evolution in the genus Homo. Journal of Human Evolution, 47(5), 279–303.

    PubMed  Google Scholar 

  • Bruner, E. (2010). Morphological differences in the parietal lobes within the human genus. Current Anthropology, 51(S1), S77–S88.

    Google Scholar 

  • Bruner, E., Manzi, G., & Arsuaga, J. L. (2003). Encephalization and allometric trajectories in the genus Homo: Evidence from the Neandertal and modern lineages. Proceedings of the National Academy of Sciences, 100(26), 15335–15340.

    CAS  Google Scholar 

  • Cave, A. J. E., & Haines, R. W. (1940). The paranasal sinuses of the anthropoid apes. Journal of Anatomy, 74(Pt 4), 493.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chan, Y. C., Roos, C., Inoue-Murayama, M., Inoue, E., Shih, C. C., & Vigilant, L. (2012). A comparative analysis of Y chromosome and mtDNA phylogenies of the Hylobates gibbons. BMC Evolutionary Biology, 12(1), 150.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clark, W. L. G., Cooper, D. M., & Zuckerman, S. (1936). The endocranial cast of the chimpanzee. Journal of the Anthropological Institute of Great Britain and Ireland, 66, 249–268.

    Google Scholar 

  • Dean, M. C. (1982). The comparative anatomy of the hominoid cranial base (Doctoral dissertation). London: University of London.

    Google Scholar 

  • Dean, M. C., & Wood, B. A. (1984). Phylogeny, neoteny and growth of the cranial base in hominoids. Folia Primatologica, 43(2–3), 157–180.

    CAS  Google Scholar 

  • Delattre, A., & Fenart, R. (1956). Remarques sur le prognathisme: sa mesure. Bulletins et Mémoires de la Société d’anthropologie de Paris, 7(3), 182–203.

    Google Scholar 

  • Dryden, I. L., & Mardia, K. V. (1998). Statistical analysis of shape. New York: Wiley.

    Google Scholar 

  • Duckworth, W. L. (1904). Morphology and anthropology, a handbook for students. Cambridge: Cambridge University Press.

    Google Scholar 

  • Durrleman, S., Pennec, X., Trouvé, A., Ayache, N., & Braga, J. (2012). Comparison of the endocranial ontogenies between chimpanzees and bonobos via temporal regression and spatiotemporal registration. Journal of Human Evolution, 62(1), 74–88.

    PubMed  Google Scholar 

  • Enlow, D. H., & Hans, M. G. (2008). Essentials of facial growth. Philadelphia: Saunders.

    Google Scholar 

  • Fooden, J., & Izor, R. J. (1983). Growth curves, dental emergence norms, and supplementary morphological observations in known-age captive orangutans. American Journal of Primatology, 5(4), 285–301.

    Google Scholar 

  • Gaul, G. (1933). Über die Wachstumsveränderungen am Gehirnschädel des Orang-Utan. Zeitschrift für Morphologie und Anthropologie, 31(3), 362–394.

    Google Scholar 

  • Giles, E. (1956). Cranial allometry in the great apes. Human Biology, 28(1), 43.

    CAS  PubMed  Google Scholar 

  • Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge: Harvard University Press.

    Google Scholar 

  • Gould, S. J. (1982). Change in developmental timing as a mechanism of macroevolution. In J. T. Bonner (Ed.), Evolution and development, Dahlem Konferenzen (pp. 333–346). New York: Springer.

    Google Scholar 

  • Gould, S. J. (2002). The structure of evolutionary theory. Cambridge: Harvard University Press.

    Google Scholar 

  • Gower, J. C. (1975). Generalized procrustes analysis. Psychometrika, 40(1), 33–51.

    Google Scholar 

  • Gunz, P. (2005). Statistical & geometric reconstruction of hominid crania reconstructing australopithecine ontogeny (Doctoral dissertation). Vienna: Universität Wien.

    Google Scholar 

  • Gunz, P., Bookstein, F. L., Mitteroecker, P., Stadlmayr, A., Seidler, H., & Weber, G. W. (2009). Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario. Proceedings of the National Academy of Sciences, 106(15), 6094–6098.

    CAS  Google Scholar 

  • Gunz, P., & Bulygina, E. (2012). The Mousterian child from Teshik-Tash is a Neanderthal: A geometric morphometric study of the frontal bone. American Journal of Physical Anthropology, 149(3), 365–379.

    PubMed  Google Scholar 

  • Gunz, P., & Mitteroecker, P. (2013). Semilandmarks: A method for quantifying curves and surfaces. Hystrix, the Italian Journal of Mammalogy, 24(1), 7.

    Google Scholar 

  • Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). New York: Springer.

    Google Scholar 

  • Gunz, P., Neubauer, S., Golovanova, L., Doronichev, V., Maureille, B., & Hublin, J. J. (2012). A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya. Journal of Human Evolution, 62(2), 300–313.

    PubMed  Google Scholar 

  • Gunz, P., Neubauer, S., Maureille, B., & Hublin, J. J. (2010). Brain development after birth differs between Neanderthals and modern humans. Current Biology, 20(21), R921–R922.

    CAS  PubMed  Google Scholar 

  • Gunz, P., Neubauer, S., Maureille, B., & Hublin, J. J. (2011). Virtual reconstruction of the Le Moustier 2 newborn skull. Implications for Neandertal ontogeny. PALEO, Revue d’archéologie préhistorique, 22, 155–172.

    Google Scholar 

  • Hens, S. M. (2002). A geometric approach to cranial sexual dimorphism in the orang-utan. Folia Primatologica, 73(4), 165–174.

    Google Scholar 

  • Hens, S. M. (2003). Growth and sexual dimorphism in orangutan crania: A three-dimensional approach. American Journal of Physical Anthropology, 121(1), 19–29.

    PubMed  Google Scholar 

  • Hrdlička, A. (1907). Anatomical observations on a collection of orang skulls from western Borneo, with a bibliography. Proceedings of the United States National Museum, 31, 539–568.

    Google Scholar 

  • Hrdlička, A. (1925). Weight of the brain and of the internal organs in American monkeys. With data on brain weight in other apes. American Journal of Physical Anthropology, 8(2), 201–211.

    Google Scholar 

  • Isler, K., Christopher Kirk, E., Miller, J., Albrecht, G. A., Gelvin, B. R., & Martin, R. D. (2008). Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. Journal of Human Evolution, 55(6), 967–978.

  • Keith, A. (1895). Growth of brain in men and monkeys, with a short criticism of the usual method of stating brain-ratios. Journal of Anatomy and Physiology, 29(Pt 2), 282.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keith, A. (1910). Description of a new craniometer and of certain age changes in the anthropoid skull. Journal of Anatomy and Physiology, 44(Pt 3), 251.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koppe, T., Röhrer-Ertl, O., Hahn, D., Reike, R., & Nagai, H. (1995). Growth pattern of the maxillary sinus in orang-utan based on measurements of CT scans. Okajimas Folia Anatomica Japonica, 72(1), 37–43.

    CAS  PubMed  Google Scholar 

  • Krogman, W. M. (1931a). Studies in growth changes in the skull and face of Anthropoids. III. Growth changes in the skull and face of the Gorilla. American Journal of Anatomy, 47(1), 89–115.

    Google Scholar 

  • Krogman, W. M. (1931b). Studies in growth changes in the skull and face of Anthropoids. IV. Growth changes in the skull and face of the Chimpanzee. American Journal of Anatomy, 47(2), 325–342.

    Google Scholar 

  • Krogman, W. M. (1931c). Studies in growth changes in the skull and face of Anthropoids. V. Growth changes in the skull and face of the Orang-utan. American Journal of Anatomy, 47(2), 343–365.

    Google Scholar 

  • Laitman, J. T., Heimbuch, R. C., & Crelin, E. S. (1978). Developmental change in a basicranial line and its relationship to the upper respiratory system in living primates. American Journal of Anatomy, 152(4), 467–482.

    CAS  PubMed  Google Scholar 

  • Leigh, S. R. (1992). Patterns of variation in the ontogeny of primate body size dimorphism. Journal of Human Evolution, 23(1), 27–50.

    Google Scholar 

  • Leigh, S. R., & Shea, B. T. (1995). Ontogeny and the evolution of adult body size dimorphism in apes. American Journal of Primatology, 36(1), 37–60.

    Google Scholar 

  • Leslie, E. R. (2010). A comparative analysis of internal cranial anatomy in the Hylobatidae. American Journal of Physical Anthropology, 143(2), 250–265.

    PubMed  Google Scholar 

  • Leutenegger, W., & Masterson, T. J. (1989a). The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus): I. Univariate analyses. Zeitschrift für Morphologie und Anthropologie, 78, 1–14.

  • Leutenegger, W., & Masterson, T. J. (1989b). The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus): II. Allometry and heterochrony. Zeitschrift für Morphologie und Anthropologie, 78, 15–24.

  • Lieberman, D. E., Krovitz, G. E., & McBratney-Owen, B. (2004). Testing hypotheses about tinkering in the fossil record: The case of the human skull. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 302(3), 284–301.

    Google Scholar 

  • Lieberman, D. E., McBratney, B. M., & Krovitz, G. (2002). The evolution and development of cranial form in Homo sapiens. Proceedings of the National Academy of Sciences, 99(3), 1134–1139.

    CAS  Google Scholar 

  • MacKinnon, J. (1974). The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Animal Behaviour, 22(1), 3–74.

    Google Scholar 

  • Masterson, T. J., & Leutenegger, W. (1992). Ontogenetic patterns of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus). Journal of Human Evolution, 23(1), 3–26.

    Google Scholar 

  • McFarlin, S. C., Barks, S. K., Tocheri, M. W., Massey, J. S., Eriksen, A. B., Fawcett, K. A., et al. (2012). Early Brain Growth Cessation in Wild Virunga Mountain Gorillas (Gorilla berengei beringei). American Journal of Primatology, 75, 450–463.

    PubMed  Google Scholar 

  • McNamara, K. J., & McKinney, M. L. (2005). Heterochrony, disparity, and macroevolution. Paleobiology, 31(sp5), 17–26.

    Google Scholar 

  • McNulty, K. P., Frost, S. R., & Strait, D. S. (2006). Examining affinities of the Taung child by developmental simulation. Journal of human evolution, 51(3), 274–296.

  • Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., & Bookstein, F. L. (2004a). Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution, 46(6), 679–698.

    PubMed  Google Scholar 

  • Mitteroecker, P., Gunz, P., & Bookstein, F. L. (2005). Heterochrony and geometric morphometrics: A comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evolution & Development, 7(3), 244–258.

    Google Scholar 

  • Mitteroecker, P., Gunz, P., Weber, G. W., & Bookstein, F. L. (2004b). Regional dissociated heterochrony in multivariate analysis. Annals of Anatomy, 186(5), 463–470.

    CAS  PubMed  Google Scholar 

  • Moss, M. L., & Young, R. W. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18(4), 281–292.

    CAS  PubMed  Google Scholar 

  • Nehm, R. H. (2001). The developmental basis of morphological disarmament in Prunum (Neogastropoda: Marginellidae). In M. L. Zelditch (Ed.), Beyond heterochrony: The evolution of development (pp. 1–26). New York: Wiley-Liss.

    Google Scholar 

  • Neubauer, S., Gunz, P., & Hublin, J. J. (2009). The pattern of endocranial ontogenetic shape changes in humans. Journal of Anatomy, 215(3), 240–255.

    PubMed Central  PubMed  Google Scholar 

  • Neubauer, S., Gunz, P., & Hublin, J. J. (2010). Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects. Journal of Human Evolution, 59(5), 555–566.

    PubMed  Google Scholar 

  • Neubauer, S., Gunz, P., Mitteroecker, P., & Weber, G. W. (2004). Three-dimensional digital imaging of the partial Australopithecus africanus endocranium MLD 37/38. Canadian Association of Radiologists Journal, 55(4), 271–277.

    PubMed  Google Scholar 

  • Neubauer, S., Gunz, P., Schwarz, U., Hublin, J. J., & Boesch, C. (2012). Brief communication: Endocranial volumes in an ontogenetic sample of chimpanzees from the Taï Forest National Park, Ivory Coast. American Journal of Physical Anthropology, 147(2), 319–325.

    PubMed  Google Scholar 

  • Neubauer, S., & Hublin, J. J. (2012). The evolution of human brain development. Evolutionary Biology, 39(4), 568–586.

    Google Scholar 

  • Randall, F. E. (1943). The skeletal and dental development and variability of the gorilla. Human Biology, 15(3), 236–254.

    Google Scholar 

  • Richtsmeier, J. T., Aldridge, K., DeLeon, V. B., Panchal, J., Kane, A. A., Marsh, J. L., et al. (2006). Phenotypic integration of neurocranium and brain. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 306(4), 360–378.

    PubMed Central  Google Scholar 

  • Richtsmeier, J. T., & Flaherty, K. (2013). Hand in glove: Brain and skull in development and dysmorphogenesis. Actaneuropathologica, 125, 1–21.

  • Richtsmeier, J. T., & Lele, S. (1993). A coordinate-free approach to the analysis of growth patterns: Models and theoretical considerations. Biological Reviews, 68(3), 381–411.

    CAS  PubMed  Google Scholar 

  • Rijksen, H. D. (1978). A fieldstudy on Sumatran orang utans (Pongo pygmaeus abelii, Lesson 1827): Ecology, behaviour and conservation. Netherlands: H. Veenman.

    Google Scholar 

  • Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39(1), 40–59.

    Google Scholar 

  • Röhrer-Ertl, O. (1988). Cranial growth. In J. L. Schwartz (Ed.), Orang-utan biology (pp. 201–223). Oxford: Oxford University Press.

    Google Scholar 

  • Ross, C., & Henneberg, M. (1995). Basicranial flexion, relative brain size, and facial kyphosis in Homo sapiens and some fossil hominids. American Journal of Physical Anthropology, 98(4), 575–593.

    CAS  PubMed  Google Scholar 

  • Ross, C. F., & Ravosa, M. J. (1993). Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. American Journal of Physical Anthropology, 91(3), 305–324.

    CAS  PubMed  Google Scholar 

  • Schultz, A. H. (1927). Studies on the growth of gorilla and of other higher primates: with special reference to a fetus of gorilla, preserved in the Carnegie Museum (Vol. 11). Memoirs of the Carnegie Museum, 11(1), 1–86 plus plates.

  • Schultz, A. H. (1940). Growth and development of the chimpanzee. Publication 518. Contributions to Embryology. Carnegie Institute, 28, 1–63.

    Google Scholar 

  • Schultz, A. H. (1944). Age changes and variability in gibbons. A Morphological study on a population sample of a man-like ape. American Journal of Physical Anthropology, 2(1), 1–129.

    Google Scholar 

  • Schultz, A. H. (1962). Metric age changes and sex differences in primate skulls. Zeitschrift für Morphologie und Anthropologie, 52(3), 239–255.

    Google Scholar 

  • Scott, J. H. (1958). The cranial base. American Journal of Physical Anthropology, 16(3), 319–348.

    CAS  PubMed  Google Scholar 

  • Selenka, E. (1898). Studien über Entwickelungsgeschichte der Thiere. Wiesbaden: CW Kreidels Verlag.

    Google Scholar 

  • Shea, B. T. (1983a). Allometry and heterochrony in the African apes. American Journal of Physical Anthropology, 62(3), 275–289.

    CAS  PubMed  Google Scholar 

  • Shea, B. T. (1983b). Size and diet in the evolution of African ape craniodental form. Folia Primatologica, 40(1–2), 32–68.

    CAS  Google Scholar 

  • Shea, B. T. (1985a). The ontogeny of sexual dimorphism in the African apes. American Journal of Primatology, 8(2), 183–188.

    Google Scholar 

  • Shea, B. T. (1985b). On aspects of skull form in African apes and orangutans, with implications for hominoid evolution. American Journal of Physical Anthropology, 68(3), 329–342.

    CAS  PubMed  Google Scholar 

  • Shea, B. T. (1986). Ontogenetic approaches to sexual dimorphism in anthropoids. Human Evolution, 1(2), 97–110.

  • Shea, B. T. (1989). Heterochrony in human evolution: The case for neoteny reconsidered. American Journal of Physical Anthropology, 32(S10), 69–101.

    Google Scholar 

  • Simpson, G. G. (1944). Tempo and mode in evolution. New York: Columbia University Press.

    Google Scholar 

  • Spoor, F. (1997). Basicranial architecture and relative brain size of Sts 5 (Australopithecus africanus) and other Plio-Pleistocene hominids. South African Journal of Science, 93, 182–186.

    Google Scholar 

  • Symington, J. (1916). Endocranial casts and brain form: A criticism of some recent speculations. Journal of Anatomy and Physiology, 50(Pt 2), 111.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taylor, A. B., & van Schaik, C. P. (2007). Variation in brain size and ecology in Pongo. Journal of Human Evolution, 52(1), 59–71.

    PubMed  Google Scholar 

  • Thalmann, O., Fischer, A., Lankester, F., Pääbo, S., & Vigilant, L. (2007). The complex evolutionary history of gorillas: Insights from genomic data. Molecular Biology and Evolution, 24(1), 146–158.

    CAS  PubMed  Google Scholar 

  • Thompson, M. E., Zhou, A., & Knott, C. D. (2012). Low testosterone correlates with delayed development in male orangutans. PLoS ONE, 7(10), e47282. doi:10.1371/journal.pone.0047282.

    CAS  Google Scholar 

  • Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York: Springer.

    Google Scholar 

  • von Baer, C. E. (1828). Über Entwicklungsgeschichte der Thiere. Beobachtung und Reflexion (Vol. 1). Königsberg: Gebrüder Bornträger.

    Google Scholar 

  • von Zieten, R. P., Gunkel, F., & Welz, B. (1987). Cranial capacity estimations of the Frankfurt Pan troglodytes verus collection. Human Evolution, 2(4), 365–372.

    Google Scholar 

  • Webster, M., Sheets, H. D., & Hughes, N. C. (2001). Allometric patterning in trilobite ontogeny: testing for heterochrony in Nepholenellus. In M. L. Zelditch (Ed.), Beyond heterochrony: The evolution of development (pp. 105–144). New York: Wiley-Liss.

    Google Scholar 

  • Weidenreich, F. (1941). The brain and its role in the phylogenetic transformation of the human skull. Transactions of the American Philosophical Society, 31(5), 320–442.

    Google Scholar 

  • Winkler, L. A., Conroy, G. C., & Vannier, M. W. (1988). Sexual dimorphism in exocranial and endocranial dimensions (pp. 225–232). Orang-utan biology. Oxford: Oxford University Press.

    Google Scholar 

  • Zelditch, M. (Ed.). (2001). Beyond heterochrony: The evolution of development. New York: Wiley-Liss.

    Google Scholar 

  • Zelditch, M. L., & Fink, W. L. (1996). Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology, 22, 241–254.

  • Zihlman, A. L., Stahl, D., & Boesch, C. (2007). Morphological variation in adult chimpanzees (Pan troglodytes verus) of the Tai National Park, Cote d’Ivoire. American Journal of Physical Anthropology, 135(1), 34–41.

    Google Scholar 

  • Zollikofer, C. P. E., & Ponce De León, M. S. (2004). Kinematics of cranial ontogeny: Heterotopy, heterochrony, and geometric morphometric analysis of growth models. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 302(3), 322–340.

    Google Scholar 

  • Zuckerman, S. (1928). Age‐changes in the Chimpanzee, with special reference to Growth of Brain, Eruption of Teeth, and Estimation of Age; with a Note on the Taungs Ape. In Proceedings of the Zoological Society of London (Vol. 98, No. 1, pp. 1–42). Oxford: Blackwell Publishing Ltd.

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Acknowledgments

The authors are grateful to C. Boesch, H. Coqueugniot, C. Feja, F. Grine, M. von Harling, B. Herzig, J. L. Kahn, the Kyoto University Primate Research Institute, N. Lange, F. Mayer, U. Olbrich-Schwartz, K. Spanel-Borowski, F. Spoor, F. Veillon, G.Weber and A. Winter for access to specimens; P. Schönfeld, P. Schubert, H. Temming and A. Winzer for CT scanning; and the Ivorian authorities, especially the Ministry of the Environment and Forests and the Ministry of Research, the Swiss Centre for Scientific Research Abidjan, and the University of Zurich for their support of the Taï chimpanzee study. The authors would like to thank A. Sylvester, A. Strauss, S. Stelzer and S. Kozakowski for helpful discussion. This research was supported by the Max Planck Society and by a Natural Sciences and Engineering Research Council of Canada Postgraduate Scholarship (NAS).

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11692_2014_9290_MOESM1_ESM.eps

Endocranial growth curves in absolute terms: non-human hominoids. Absolute endocranial volumes are plotted against age groups as coloured filled circles. Volume growth curves are shown as dashed lines, cubed centroid size growth curves as solid lines. (EPS 1108 kb)

11692_2014_9290_MOESM2_ESM.eps

Ontogenetic shape trajectories as ontogenetic sequences of specimens in shape space: non-human great apes. PCA of Procrustes shape variables from the eruption of deciduous dentition (age group 2) to adulthood (age group 6). A: The projection of principal components one and two; B: The projection of principal components one and three. Cumulative explained variance for the first three principal components is 64 %. Borderless convex hulls represent pooled sexes of age groups 2-6 for each species; convex hulls with dashed borders represent adult females, those with solid borders represent adult males. Age group labels denote age group means. Lines are B-spline curves of the average species-specific trajectories. Endocranial shape variation along the first three PCs is visualized as mean shapes ± two standard deviations (± 2 SDVs) from the sample mean. (EPS 1656 kb)

Classification accuracy of developmental simulations. (XLSX 12 kb)

Shape change in humans along entire trajectory in fig. 5b. (MPG 2156 kb)

Shape change in humans between age groups 2 and 3 in fig. 5b, exaggeration factor: 2. (MPG 735 kb)

Shape change in humans between age groups 3 and 4 in fig. 5b, exaggeration factor: 2. (MPG 735 kb)

Shape change in humans between age groups 4 and 6 in fig. 5b, exaggeration factor: 2. (MPG 730 kb)

Shape change in chimpanzees along entire trajectory in fig. 5b. (MPG 2886 kb)

Shape change in chimpanzees between age groups 2 and 3 in fig. 5b, exaggeration factor: 2. (MPG 737 kb)

Shape change in chimpanzees between age groups 3 and 4 in fig. 5b, exaggeration factor: 2. (MPG 730 kb)

Shape change in chimpanzees between age groups 4 and 5 in fig. 5b, exaggeration factor: 2. (MPG 739 kb)

Shape change in chimpanzees between age groups 5 and 6 in fig. 5b, exaggeration factor: 2. (MPG 739 kb)

Shape change in gorillas along entire trajectory in fig. 5b. (MPG 2889 kb)

Shape change in gorillas between age groups 2 and 3 in fig. 5b, exaggeration factor: 2. (MPG 739 kb)

Shape change in gorillas between age groups 3 and 4 in fig. 5b, exaggeration factor: 2. (MPG 739 kb)

Shape change in gorillas between age groups 4 and 5 in fig. 5b, exaggeration factor: 2. (MPG 739 kb)

Shape change in gorillas between age groups 5 and 6 in fig. 5b, exaggeration factor: 2. (MPG 739 kb)

Shape change in orangutans along entire trajectory in fig. 5b. (MPG 2895 kb)

Shape change in orangutans between age groups 2 and 3 in fig. 5b, exaggeration factor: 2. (MPG 737 kb)

Shape change in orangutans between age groups 3 and 4 in fig. 5b, exaggeration factor: 2. (MPG 737 kb)

Shape change in orangutans between age groups 4 and 5 in fig. 5b, exaggeration factor: 2. (MPG 733 kb)

Shape change in orangutans between age groups 5 and 6 in fig. 5b, exaggeration factor: 2. (MPG 742 kb)

Shape change in gibbons along entire trajectory in fig. 5b. (MPG 1436 kb)

Shape change in gibbons between age groups 4 and 5 in fig. 5b, exaggeration factor: 2. (MPG 735 kb)

Shape change in gibbons between age groups 5 and 6 in fig. 5b, exaggeration factor: 2. (MPG 737 kb)

11692_2014_9290_MOESM26_ESM.cdf

Ontogenetic trajectories in age-shape-size space. Trajectories are constructed as accumulations of mean differences in shape (Procrustes distance) and size (endocranial volume difference) for each age group transition. All trajectories begin at a common origin (grey sphere). Gibbons were excluded from this analysis as only those species represented from age group 2 onwards were included. Blue spheres denote humans, orange denotes gorilla, green denotes chimpanzees and red denotes orangutans. (CDF 5 kb)

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Scott, N., Neubauer, S., Hublin, JJ. et al. A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids. Evol Biol 41, 572–594 (2014). https://doi.org/10.1007/s11692-014-9290-7

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