Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects

Journal of Human Evolution

Volumn 59, Issue 5, 2010, Pages 555-566

  Neubauer, Simon ^a   Gunz, Philipp ^a   Hublin, Jean Jacques ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

Brain; Geometric morphometrics; Hominin evolution; Ontogeny; Semilandmarks; Virtual endocasts

Indexed keywords

BRAIN; CRANIUM; HOMINID; HUMAN EVOLUTION; MORPHOMETRY; ONTOGENY; SHAPE; TOMOGRAPHY;

PAN;

EID: 77958177712     PISSN: 00472484     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhevol.2010.06.011     Document Type: Article

References (115)

1. Ackermann R.R., Krovitz G.E. Common patterns of facial ontogeny in the hominid lineage. Anat. Rec. 2002, 269:142-147.
2. Bastir M., Rosas A. Comparative ontogeny in humans and chimpanzees: similarities, differences and paradoxes in postnatal growth and development of the skull. Ann. Anat. 2004, 186:503-509.
3. Bastir M., Rosas A. Hierarchical nature of morphological integration and modularity in the human posterior face. Am. J. Phys. Anthropol. 2005, 128:26-34.
4. Bastir M., Rosas A. Correlated variation between the lateral basicranium and the face: a geometric morphometric study in different human groups. Arch. Oral Biol. 2006, 51:814-824.
5. Bastir M., Rosas A. Mosaic evolution of the basicranium in Homo and its relation to modular development. Evol. Biol. 2009, 36:57-70.
6. Bastir M., Rosas A., Kuroe K. Petrosal orientation and mandibular ramus breadth: evidence for an integrated petroso-mandibular developmental unit. Am. J. Phys. Anthropol. 2004, 123:340-350.
7. Bastir M., Rosas A., Lieberman D.E., O'Higgins P. Middle cranial fossa anatomy and the origin of modern humans. Anat. Rec. 2008, 291:130-140.
8. Bastir M., Rosas A., O'Higgins P. Craniofacial levels and the morphological maturation of the human skull. J. Anat. 2006, 209:637-654.
9. Bastir M., Rosas A., Stringer C., Manuel Cuétara J., Kruszynski R., Weber G.W., Ross C.F., Ravosa M.J. Effects of brain and facial size on basicranial form in human and primate evolution. J. Hum. Evol. 2010, 58:424-431.
10. Bastir M., Rosas A., Tabernero A.G., Peña-Melián A., Estalrrich A., de la Rasilla M., Fortea J. Comparative morphology and morphometric assessment of the Neandertal occipital remains from the El Sidrón site (Asturias, Spain: years 2000-2008). J. Hum. Evol. 2010, 58:68-78.
11. Biegert J. The evaluation of characteristics of the skull, hands and feet for primate taxonomy. Classification and Human Evolution 1963, 116-145. Aldine De Gruyter, Chicago. S.L. Washburn (Ed.).
12. Boas F. The growth of children. Science 1892, 19:256-257.
13. Bookstein F.L. Morphometric Tools for Landmark Data: Geometry and Biology 1991, Cambridge University Press, Cambridge.
14. Bookstein F.L. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1997, 1:225-243.
15. Bookstein F., Schäfer K., Prossinger H., Seidler H., Fieder M., Stringer C., Weber G.W., Arsuaga J.-L., Slice D.E., Rohlf F.J., Recheis W., Mariam A.J., Marcus L.F. Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Anat. Rec. 1999, 257:217-224.
16. Bruner E. Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J. Hum. Evol. 2004, 47:279-303.
17. Bruner E., Manzi G. Allometric analysis of the skull in Pan and Gorilla by geometric morphometrics. Riv. Antropol. 2001, 79:45-52.
18. Bruner E., Ripani M. A quantitative and descriptive approach to morphological variation of the endocranial base in modern humans. Am. J. Phys. Anthropol. 2008, 137:30-40.
19. Bruner E., Manzi G., Arsuaga J.L. Encephalization and allometric trajectories in the genus Homo: evidence from the Neandertal and modern lineages. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15335-15340.
20. Bruner E., Martin-Loeches M., Colom R. Human midsagittal brain shape variation: patterns, allometry and integration. J. Anat. 2010, 216:589-599.
21. Bulygina E., Mitteroecker P., Aiello L. Ontogeny of facial dimorphism and patterns of individual development within one human population. Am. J. Phys. Anthropol. 2006, 131:432-443.
22. Buschang P.H., Baume R.M., Nass G.G. A craniofacial growth maturity gradient for males and females between 4 and 16 years of age. Am. J. Phys. Anthropol. 1983, 61:373-381.
23. Casey B.J., Tottenham N., Liston C., Durston S. Imaging the developing brain: what have we learned about cognitive development?. Trends Cogn. Sci. 2005, 9:104-110.
24. Cobb S.N., O'Higgins P. Hominins do not share a common postnatal facial ontogenetic shape trajectory. J. Exp. Zoolog. B. Mol. Dev. Evol. 2004, 302:302-321.
25. Cobb S.N., O'Higgins P. The ontogeny of sexual dimorphism in the facial skeleton of the African apes. J. Hum. Evol. 2007, 53:176-190.
26. Coqueugniot H., Hublin J.J., Veillon F., Houët F., Jacob T. Early brain growth in Homo erectus and implications for cognitive ability. Nature 2004, 431:299-302.
27. Courchesne E., Pierce K. Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connectivity. Int. J. Dev. Neurosci. 2005, 23:153-170.
28. Courchesne E., Carper R., Akshoomoff N. Evidence of brain overgrowth in the first year of life in autism. JAMA 2003, 290:337-344.
29. Courchesne E., Pierce K., Schumann C.M., Redcay E., Buckwalter J.A., Kennedy D.P., Morgan J. Mapping early brain development in autism. Neuron 2007, 56:399-413.
30. Dabelow A. Über Korrelationen in der phylogenetischen Entwicklung der Schädelform. I. Die Beziehungen zwischen Rumpf und Schadelform. Gegenb. Morph. Jahrb. 1929, 63:1-49.
31. Dabelow A. Über Korrelationen in der phylogenetischen Entwicklung der Schadelform. II. Beziehungen zwischen Gehirn und Schädelbasisform bei den Mammaliern. Gegenb. Morph. Jahrb. 1931, 67:84-133.
32. Dean M.C. Growth processes in the cranial base of hominoids and their bearing on morphological similarities that in the cranial base of Homo and Paranthropus. Evolutionary History of the "Robust" Australopithecines 1988, 107-112. Aldine Publ. Co., New York. F.E. Grine (Ed.).
33. DeSilva J., Lesnik J. Chimpanzee neonatal brain size: implications for brain growth in Homo erectus. J. Hum. Evol. 2006, 51:207-212.
34. Enlow D.H. The Human Face 1968, Harper & Row, New York, NY.
35. Enlow D.H. Facial Growth 1990, Saunders, Philadelphia.
36. Falk D. Hominid brain evolution: the approach from paleoneurology. Yearb. Phys. Anthropol. 1980, 23:93-107.
37. Falk D. Endocranial casts and their significance for primate brain evolution. Systematics, Evolution, and Anatomy 1986, vol. 1:477-490. Alan R. Liss, New York. D.R. Swindler, J. Erwin (Eds.).
38. Falk D. Hominid paleoneurology. Ann. Rev. Anthropol. 1987, 16:13-28.
39. Gale C.R., O'Callaghan F.J., Godfrey K.M., Law C.M., Martyn C.N. Critical periods of brain growth and cognitive function in children. Brain 2004, 127:321-329.
40. Giedd J.N. Structural magnetic resonance imaging of the adolescent brain. Ann. N.Y. Acad. Sci. 2004, 1021:77-85.
41. Godfrey L.R., Sutherland M.R. Paradox of peramorphic paedomorphosis: heterochrony and human evolution. Am. J. Phys. Anthropol. 1996, 99:17-42.
42. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8174-8179.
43. Gould S.J. Ontogeny and Phylogeny 1977, Belknap Press of Harvard University Press, Cambridge.
44. Gower J.C. Generalized Procrustes analysis. Pyschometrika 1975, 40:33-51.
45. Grine F.E., Gunz P., Betti-Nash L., Neubauer S., Morris A.G. Reconstruction of the Late Pleistocene human skull from Hofmeyr, South Africa. J. Hum. Evol. 2010, 59:1-15.
46. Gunz P., Mitteroecker P., Bookstein F.L. Semilandmarks in Three Dimensions. Modern Morphometrics in Physical Anthropology 2005, 73-98. Kluwer Academic/Plenum Publishers, New York. D.E. Slice (Ed.).
47. Gunz P., Bookstein F.L., Mitteroecker P., Stadlmayr A., Seidler H., Weber G.W. Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6094-6098.
48. Gunz P., Mitteroecker P., Neubauer S., Weber G.W., Bookstein F.L. Principles for the virtual reconstruction of hominin crania. J. Hum. Evol. 2009, 57:48-62.
49. Hallgrimsson B., Lieberman D.E. Mouse models and the evolutionary developmental biology of the skull. Integr. Comp. Biol. 2008, 48:373-384.
50. Herschkowitz N. Neurological bases of behavioral development in infancy. Brain Dev. 2000, 22:411-416.
51. Holloway R.L. The Relevance of Endocasts for Studying Primate Brain Evolution. Sensory Systems of Primates 1978, 181-200. Plenum Press, New York. C.R. Noback (Ed.).
52. Holloway R.L., Broadfield D.C., Yuan M.S. The Human Fossil Record: Brain Endocasts, the Paleoneurological Evidence 2004, Wiley-Liss, Hoboken, New Jersey.
53. Holt A.B., Cheek D.B., Mellits E.D., Hill D.E. Brain size and the relation of the primate to the nonprimate. Foetal and Postnatal Cellular Growth: Hormones and Nutrition 1975, 23-44. Wiley, New York. D.B. Cheek (Ed.).
54. Hublin J.J., Coqueugniot H. Absolute or proportional brain size: that is the question. A reply to Leigh's (2006) comments. J. Hum. Evol. 2006, 50:109-113.
55. Humphrey L.T. Growth patterns in the modern human skeleton. Am. J. Phys. Anthropol. 1998, 105:57-72.
56. Jeffery N. Brain expansion and comparative prenatal ontogeny of the non-hominoid primate cranial base. J. Hum. Evol. 2003, 45:263-284.
57. Jeffery N. Cranial base angulation and growth of the human fetal pharynx. Anat. Rec. A. Discov. Mol. Cell. Evol. Biol. 2005, 284:491-499.
58. Jeffery N., Spoor F. Brain size and the human cranial base: a prenatal perspective. Am. J. Phys. Anthropol. 2002, 118:324-340.
59. Jeffery N., Spoor F. Ossification and midline shape changes of the human fetal cranial base. Am. J. Phys. Anthropol. 2004, 123:78-90.
60. Jolicoeur P., Baron G., Cabana T. Cross-sectional growth and decline of human stature and brain weight in 19th-century Germany. Growth Dev. Aging 1988, 52:201-206.
61. Kennedy G.E. From the ape's dilemma to the weanling's dilemma: early weaning and its evolutionary context. J. Hum. Evol. 2005, 48:123-145.
62. Laitman J.T., Crelin E.S. Postnatal development of the basicranium and vocal tract region in man. Symposium on Development of the Basicranium 1976, 206-219. U.S. Department of Health, Education and Welfare, Bethesda, Maryland. J.F. Bosma (Ed.).
63. Laitman J.T., Heimbuch R.C. The basicranium of Plio-Pleistocene hominids as an indicator of their upper respiratory systems. Am. J. Phys. Anthropol. 1982, 59:323-343.
64. Leigh S.R. Brain growth, life history, and cognition in primate and human evolution. Am. J. Primatol. 2004, 62:139-164.
65. Leigh S.R. Brain ontogeny and life history in Homo erectus. J. Hum. Evol. 2006, 50:104-108.
66. Lieberman D.E., McCarthy R.C. The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. J. Hum. Evol. 1999, 36:487-517.
67. Lieberman D.E., McBratney B.M., Krovitz G. The evolution and development of cranial form in Homo sapiens. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1134-1139.
68. Lieberman D.E., Hallgrímsson B., Liu W., Parsons T.E., Jamniczky H.A. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J. Anat. 2008, 212:720-735.
69. Lieberman P., Klatt D.H., Crelin E.S. Phonetic ability and related anatomy of newborn and adult human, Neanderthal man, and chimpanzee. Am. Anthropol. 1972, 74:287-307.
70. Martin R.D. Human Brain Evolution in an Ecological Context. 52nd James Arthur Lecture on the Evolution of the Human Brain 1983, American Museum of Natural History, New York.
71. McNulty K.P., Frost S.R., Strait D.S. Examining affinities of the Taung child by developmental simulation. J. Hum. Evol. 2006, 51:274-296.
72. Mitteroecker P., Gunz P. Advances in geometric morphometrics. Evol. Biol. 2009, 36:235-247.
73. Mitteroecker P., Huttegger S.M. The concept of morphospaces in evolutionary and developmental biology: mathematics and metaphors. Biol. Theory 2009, 4:54-67.
74. Mitteroecker P., Gunz P., Bernhard M., Schaefer K., Bookstein F.L. Comparison of cranial ontogenetic trajectories among great apes and humans. J. Hum. Evol. 2004, 46:679-697.
75. Mitteroecker P., Gunz P., Bookstein F.L. Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evol. Dev. 2005, 7:244-258.
76. Mitteroecker P., Gunz P., Weber G.W., Bookstein F.L. Regional dissociated heterochrony in multivariate analysis. Ann. Anat. 2004, 186:463-470.
77. Moss M.L., Young R.W. A functional approach to craniology. Am. J. Phys. Anthropol. 1960, 18:281-292.
78. Nagy Z., Westerberg H., Klingberg T. Maturation of white matter is associated with the development of cognitive functions during childhood. J. Cogn. Neurosci. 2004, 16:1227-1233.
79. Neubauer S., Gunz P., Hublin J.J. The pattern of endocranial ontogenetic shape changes in humans. J. Anat. 2009, 215:240-255.
80. O'Higgins P., Bastir M., Kupczik K. Shaping the human face. Int. Congress Ser. 2006, 55-73.
81. Olesen P.J., Nagy Z., Westerberg H., Klingberg T. Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Brain Res. Cogn. Brain Res. 2003, 18:48-57.
82. Penin X., Berge C., Baylac M. Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional Procrustes analysis. Am. J. Phys. Anthropol. 2002, 118:50-62.
83. Perez S.I., Bernal V., Gonzalez P.N. Differences between sliding semi-landmark methods in geometric morphometrics, with an application to human craniofacial and dental variation. J. Anat. 2006, 208:769-784.
84. Ponce de León M.S., Zollikofer C.P. Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 2001, 412:534-538.
85. Rice S.H. The analysis of ontogenetic trajectories: when a change in size or shape is not heterochrony. Proc. Natl. Acad. Sci. U.S.A 1997, 94:907-912.
86. Rice S.H. The role of heterochrony in primate brain evolution. Human Evolution through Developmental Change 2001, 154-170. Johns Hopkins University Press, Baltimore. N. Minugh-Purvis, J. McNamara (Eds.).
87. Richtsmeier J.T., Lele S. A coordinate-free approach to the analysis of growth patterns: models and theoretical considerations. Biol. Rev. Camb. Philos. Soc. 1993, 68:381-411.
88. Richtsmeier J.T., Walker A. A morphometric study of facial growth. The Nariokotome Homo erectus Skeleton 1993, 391-410. Harvard University Press, Cambridge, MA. A. Walker, R. Leakey (Eds.).
89. Robson S.L., Wood B. Hominin life history: reconstruction and evolution. J. Anat. 2008, 212:394-425.
90. Rohlf F.J., Slice D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 1990, 39:40-59.
91. Rosas A., Bastir M., Martinez-Maza C., Garcia-Tabernero A., Lalueza-Fox C. Inquiries into Neanderthal craniofacial development and evolution: "accretion" versus "organismic" models. Neanderthals Revisited: New Approaches and Perspectives 2006, 37-69. Springer, New York. T. Harrison, K. Harvati (Eds.).
92. Ross C., Henneberg M. Basicranial flexion, relative brain size, and facial kyphosis in Homo sapiens and some fossil hominids. Am. J. Phys. Anthropol. 1995, 98:575-593.
93. Ross C.F., Ravosa M.J. Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. Am. J. Phys. Anthropol. 1993, 91:305-324.
94. Schultz A.H. Age changes in primates and their modification in man. Human Growth 1960, 1-20. Pergamon, Oxford. J.M. Tanner (Ed.).
95. Shea B.T. Heterochrony in human evolution: the case for neoteny reconsidered. Am. J. Phys. Anthropol. 1989, 80:69-101.
96. Slice D.E. Geometric morphometrics. Ann. Rev. Anthropol. 2007, 36:261-281.
97. Smith B.H. Dental development as a measure of life history in primates. Evolution 1989, 43:683-688.
98. Smith B.H., Tompkins R.L. Toward a life history of the Hominidae. Ann. Rev. Anthropol. 1995, 24:257-279.
99. Smith B.H., Crummett T.L., Brandt K.L. Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories. Yearb. Phys. Anthropol. 1994, 37:177-231.
100. Smith R.J., Gannon P.J., Smith B.H. Ontogeny of australopithecines and early Homo: evidence from cranial capacity and dental eruption. J. Hum. Evol. 1995, 29:155-168.
101. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nat. Neurosci. 2003, 6:309-315.
102. Sowell E.R., Thompson P.M., Leonard C.M., Welcome S.E., Kan E., Toga A.W. Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 2004, 24:8223-8231.
103. Specht M., Lebrun R., Zollikofer C.P.E. Visualizing shape transformation between chimpanzee and human braincases. Vis. Comput. 2007, 23:743-751.
104. Sperber G.H. Craniofacial Embryology 1989, John Wright, London.
105. Spoor F. Basicranial architecture and relative brain size of Sts 5 (Australopithecus africanus) and other Plio-Pleistocene hominids. S. Afr. J. Sci. 1997, 93:182-186.
106. Tanner J.M. Foetus into Man 1978, Harvard University Press, Cambridge.
107. Trenouth M.J., Timms D.J. Relationship of the functional oropharynx to craniofacial morphology. Angle. Orthod. 1999, 69:419-423.
108. Vi{eth}arsdóttir U.S., Cobb S. Inter- and intra-specific variation in the ontogeny of the hominoid facial skeleton: testing assumptions of ontogenetic variability. Ann. Anat. 2004, 186:423-428.
109. Vi{eth}arsdóttir U.S., O'Higgins P., Stringer C. A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton. J. Anat. 2002, 201:211-229.
110. Vinicius L. Human encephalization and developmental timing. J. Hum. Evol. 2005, 49:762-776.
111. Vinicius L., Lahr M.M. Morphometric heterochrony and the evolution of growth. Evolution 2003, 57:2459-2468.
112. Vrba E.S. Multiphasic growth models and the evolution of prolonged growth exemplified by human brain evolution. J. Theor. Biol. 1998, 190:227-239.
113. Weidenreich F. The brain and its role in the phylogenetic transformation of the human skull. Trans. Amer. Phil. Soc. 1941, 31:321-442.
114. White T.D., Asfaw B., Beyene Y., Haile-Selassie Y., Lovejoy C.O., Suwa G., WoldeGabriel G. Ardipithecus ramidus and the paleobiology of early hominids. Science 2009, 326:75-86.
115. Zollikofer C.P.E., Ponce de León M.S. Kinematics of cranial ontogeny: heterotopy, heterochrony, and geometric morphometric analysis of growth models. J. Exp. Zool. B. 2004, 302:322-340.