Ontogenetic and static allometry in the human face: Contrasting Khoisan and Inuit

American Journal of Physical Anthropology

Volumn 158, Issue 1, 2015, Pages 116-131

  Freidline, Sarah E ^a   Gunz, Philipp ^a   Hublin, Jean Jacques ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

heterochrony; Inuit; Khoisan; midface; ontogenetic allometry; Point Hope; semilandmark geometric morphometrics; static allometry

Indexed keywords

ADOLESCENT; ADULT; ALLOMETRY; ARTICLE; CHILD; CRANIOFACIAL MORPHOLOGY; FACE; FACE DEVELOPMENT; FACE GROWTH; FEMALE; GROWTH RATE; HUMAN; INUIT; KHOISAN; MALE; ONTOGENY; POSTNATAL DEVELOPMENT; SEX DIFFERENCE; ANATOMY AND HISTOLOGY; ANCESTRY GROUP; ANTHROPOMETRY; CROSS-SECTIONAL STUDY; FACIAL BONE; PHYSICAL ANTHROPOLOGY; PRESCHOOL CHILD; PRINCIPAL COMPONENT ANALYSIS; PROCEDURES; STATISTICS AND NUMERICAL DATA; YOUNG ADULT;

ADOLESCENT; ADULT; ANTHROPOLOGY, PHYSICAL; ANTHROPOMETRY; CHILD; CHILD, PRESCHOOL; CONTINENTAL POPULATION GROUPS; CROSS-SECTIONAL STUDIES; FACE; FACIAL BONES; FEMALE; HUMANS; MALE; PRINCIPAL COMPONENT ANALYSIS; YOUNG ADULT;

EID: 84938962637     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22759     Document Type: Article

References (107)

1. Ackermann RR, Krovitz GE,. 2002. Common patterns of facial ontogeny in the hominid lineage. Anat Rec 269: 142-147.
2. Alberch P, Gould SJ, Oster GF, Wake DB,. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5: 296-317.
3. Athreya S,. 2009. A comparative study of frontal bone morphology among pleistocene hominin fossil groups. J Hum Evol 57: 786-804.
4. Bastir M,. 2008. A systems-model for the morphological analysis of integration and modularity in human craniofacial evolution. J Anthropol Sci 86: 37-58.
5. Bastir M, Godoy P, Rosas A,. 2011. Common features of sexual dimorphism in the cranial airways of different human populations. Am J Phys Anthropol 146: 414-422.
6. Bastir M, Rosas A,. 2004. Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. J Hum Evol 47: 359-381.
7. Bastir M, Rosas A,. 2005. Hierarchical nature of morphological integration and modularity in the human posterior face. Am J Phys Anthropol 128: 26-34.
8. Bastir M, Rosas A, O'Higgins P,. 2006. Craniofacial levels and the morphological maturation of the human skull. J Anat 209: 637-654.
9. Baughan B, Demirjian A, Levesque GY, Lapalme-Chaput L,. 1979. The pattern of facial growth before and during puberty, as shown by French-canadian girls. Ann Hum Biol 6: 59-76.
10. Bjork A, Skieller V,. 1972. Facial development and tooth eruption. An implant study at the age of puberty. Am J Orthod 62: 339-383.
11. Bulygina E, Mitteroecker P, Aiello L,. 2006. Ontogeny of facial dimorphism and patterns of individual development within one human population. Am J Phys Anthropol 131: 432-443.
12. Buschang PH, Baume RM, Nass GG,. 1983. A craniofacial growth maturity gradient for males and females between 4 and 16 years of age. Am J Phys Anthropol 61: 373-381.
13. Carey JW, Steegmann AT Jr., 1981. Human nasal protrusion, latitude, and climate. Am J Phys Anthropol 56: 313-319.
14. Cheverud JM,. 1982. Relationships among ontogenetic, static, and evolutionary allometry. Am J Phys Anthropol 59: 139-149.
15. Cobb SN, O'Higgins P,. 2004. Hominins do not share a common postnatal facial ontogenetic shape trajectory. J Exp Zool B Mol Dev Evol 302: 302-321.
16. Cock AG,. 1966. Genetical aspects of metrical growth and form in animals. Q Rev Biol 41: 131-190.
17. Coquerelle M, Bookstein FL, Braga J, Halazonetis DJ, Weber GW, Mitteroecker P,. 2011. Sexual dimorphism of the human mandible and its association with dental development. Am J Phys Anthropol 145: 192-202.
18. Dressino V, Pucciarelli HM,. 1997. Cranial growth in Saimiri sciureus (cebidae) and its alteration by nutritional factors: a longitudinal study. Am J Phys Anthropol 102: 545-554.
19. Dryden IL, Mardia KV., 1998. Statistical shape analysis. Chichester: John Wiley & Sons.
20. Enlow DH., 1990. Facial growth. Philadelphia, PA: W. B. Saunders Company.
21. Enlow DH, Hans MG., 2008. Essentials of facial growth. Ann Arbor, MI: Needham Press.
22. Franciscus RG, Trinkaus E,. 1988. Nasal morphology and the emergence of homo erectus. Am J Phys Anthropol 75: 517-527.
23. Freidline SE, Gunz P, Harvati K, Hublin J-J,. 2012a. Middle pleistocene human facial morphology in an evolutionary and developmental context. J Hum Evol 63: 723-740.
24. Freidline SE, Gunz P, Harvati K, Hublin J-J,. 2013. Evaluating developmental shape changes in homo antecessor subadult facial morphology. J Hum Evol 65: 404-423.
25. Freidline SE, Gunz P, Jankovic I, Harvati K, Hublin JJ,. 2012b. A comprehensive morphometric analysis of the frontal and zygomatic bone of the zuttiyeh fossil from Israel. J Hum Evol 62: 225-241.
26. Froment A,. 1992. Correspondence between anatomical differentiation and geographic distribution of modern humans studied by craniometry. CR Acad Des Sci Serie III Sci La Vie-Life Sci 315: 323-329.
27. Gonzalez PN, Kristensen E, Morck DW, Boyd S, Hallgrimsson B,. 2013. Effects of growth hormone on the ontogenetic allometry of craniofacial bones. Evol Dev 15: 133-145.
28. Gonzalez PN, Oyhenart EE, Hallgrimsson B,. 2011. Effects of environmental perturbations during postnatal development on the phenotypic integration of the skull. J Exp Zool B Mol Dev Evol 316: 547-561.
29. Gonzalez PN, Perez SI, Bernal V,. 2010. Ontogeny of robusticity of craniofacial traits in modern humans: a study of South American populations. Am J Phys Anthropol 142: 367-379.
30. Good P., 2000. Permutation tests: a practical guide to resampling methods for testing hypotheses, 2nd ed. New York: Springer.
31. Gould SJ,. 1966. Allometry and size in ontogeny and phylogeny. Biol Rev Camb Philos Soc 41: 587-640.
32. Gould SJ,. 1975. Allometry in primates, with emphasis on scaling and the evolution of the brain. Contrib Primatol 5: 244-292.
33. Gould SJ., 1977. Ontogeny and phylogeny. Cambridge: Belknap Press of Harvard University.
34. Grine FE, Gunz P, Betti-Nash L, Neubauer S, Morris AG,. 2010. Reconstruction of the late pleistocene human skull from Hofmeyr, South Africa. J Hum Evol 59: 1-15.
35. Gunz P., 2005. Statistical and geometric reconstruction of hominid crania: reconstructing australopithecine ontogeny. Vienna: University of Vienna.
36. Gunz P, Bookstein FL, Mitteroecker P, Stadlmayr A, Seidler H, Weber GW,. 2009a. Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario. Proc Natl Acad Sci USA 106: 6094-6098.
37. Gunz P, Harvati K,. 2007. The neanderthal "chignon": variation, integration, and homology. J Hum Evol 52: 262-274.
38. Gunz P, Mitteroecker P, Bookstein F., 2005. Semilandmarks in three dimensions. In:, Slice DE, editor. Modern morphometrics in physical anthropology. New York: Plenum Publishers. p 73-98.
39. Gunz P, Mitteroecker P, Neubauer S, Weber GW, Bookstein FL,. 2009b. Principles for the virtual reconstruction of hominin crania. J Hum Evol 57: 48-62.
40. Gunz P, Neubauer S, Golovanova L, Doronichev V, Maureille B, Hublin JJ,. 2012. A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the neandertal newborn from mezmaiskaya. J Hum Evol 62: 300-313.
41. Gunz P, Neubauer S, Maureille B, Hublin J-J,. 2010. Brain development after birth differs between neanderthals and modern humans. Curr Biol 20: R921-922.
42. Hall RL,. 2005. Energetics of nose and mouth breathing, body size, body composition, and nose volume in young adult males and females. Am J Hum Biol 17: 321-330.
43. Hanihara T,. 1996. Comparison of craniofacial features of major human groups. Am J Phys Anthropol 99: 389-412.
44. Hanihara T,. 2000. Frontal and facial flatness of major human populations. Am J Phys Anthropol 111: 105-134.
45. Harvati K, Hublin J-J, Gunz P,. 2010. Evolution of middle-late pleistocene human cranio-facial form: a 3-D approach. J Hum Evol 59: 445-464.
46. Hennessy RJ, Stringer CB,. 2002. Geometric morphometric study of the regional variation of modern human craniofacial form. Am J Phys Anthropol 117: 37-48.
47. Holton NE, Yokley TR, Froehle AW, Southard TE,. 2014. Ontogenetic scaling of the human nose in a longitudinal sample: implications for genus homo facial evolution. Am J Phys Anthropol 153: 52-60.
48. Howells WW., 1973. Cranial variation in man: a study by multivariate analysis of patterns of differences among recent human populations. Harvard, Cambridge: Papers of the Peabody Museum of Archaeology and Ethnology.
49. Howells WW., 1989. Skull shapes and the map. Harvard, Cambridge: Papers of the Peabody Museum of Archaeology and Ethnology. p 79.
50. Humphrey LT,. 1998. Growth patterns in the modern human skeleton. Am J Phys Anthropol 105: 57-72.
51. Jeffery N, Spoor F,. 2004. Prenatal growth and development of the modern human labyrinth. J Anat 204: 71-92.
52. Kappeler L, De Magalhaes Filho C, Leneuve P, Xu J, Brunel N, Chatziantoniou C, Le Bouc Y, Holzenberger M,. 2009. Early postnatal nutrition determines somatotropic function in mice. Endocrinology 150: 314-323.
53. Klingenberg CP,. 1998. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev Camb Philos Soc 73: 79-123.
54. Klingenberg CP, Zimmermann M,. 1992. Static, ontogenetic, and evolutionary allometry: a multivariate comparison in nine species of water striders. Am Nat 601-620.
55. Krovitz GE., 2003. Shape and growth differences between Neandertals and modern: grounds for a species-level distinction. In:, Thompson JL, Krovtiz G, Nelson AJ, editors. Patterns of growth and development in the genus Homo. Cambridge: Cambridge University Press. p 320-342.
56. Lahr MM, Wright RVS,. 1996. The question of robusticity and the relationship between cranial size and shape in Homo sapiens. J Hum Evol 31: 157-191.
57. Lieberman DE,. 1996. How and why humans grow thin skulls: experimental evidence for systemic cortical robusticity. Am J Phys Anthropol 101: 217-236.
58. Lieberman DE, Hallgrimsson B, Liu W, Parsons TE, Jamniczky HA,. 2008. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J Anat 212: 720-735.
59. Lieberman DE, McBratney BM, Krovitz G,. 2002. The evolution and development of cranial form in homo sapiens. Proc Natl Acad Sci USA 99: 1134-1139.
60. Lieberman DE, McCarthy RC,. 1999. The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. J Hum Evol 36: 487-517.
61. Lieberman DE, Ross CF, Ravosa MJ,. 2000. The primate cranial base: ontogeny, function, and integration. Am J Phys Anthropol Suppl 31: 117-169.
62. Luboga SA, Wood BA,. 1990. Position and orientation of the foramen magnum in higher primates. Am J Phys Anthropol 81: 67-76.
63. Lynch JM, Wood CG, Luboga SA,. 1996. Geometric morphometrics in primatology: craniofacial variation in homo sapiens and pan troglodytes. Folia Primatol (Basel) 67: 15-39.
64. Maddux SD., 2011. A quantitative assessment of infraorbital morphology in Homo: testing for character independence and evolutionary significance in the human midface. IA: University of Iowa.
65. Maddux SD, Franciscus RG,. 2009. Allometric scaling of infraorbital surface topography in homo. J Hum Evol 56: 161-174.
66. Martin MA, Serradas P, Ramos S, Fernandez E, Goya L, Gangnerau MN, Lacorne M, Pascual-Leone AM, Escriva F, Portha B,., et al. 2005. Protein-caloric food restriction affects insulin-like growth factor system in fetal wistar rat. Endocrinology 146: 1364-1371.
67. Martinez-Maza C, Rosas A, Nieto-Díaz M,. 2013. Postnatal changes in the growth dynamics of the human face revealed from bone modelling patterns. J Anat 223: 228-241.
68. McCollum MA,. 2008. Nasomaxillary remodeling and facial form in robust Australopithecus: a reassessment. J Hum Evol 54: 2-14.
69. McNulty KP, Frost SR, Strait DS,. 2006. Examining affinities of the Taung child by developmental simulation. J Hum Evol 51: 274-296.
70. Miller JP, German RZ,. 1999. Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr 129: 2061-2069.
71. Mitteroecker P, Gunz P,. 2009. Advances in geometric morphometrics. Evol Biol 36: 235-247.
72. Mitteroecker P, Gunz P, Bernhard M, Schaefer K, Bookstein FL,. 2004a. Comparison of cranial ontogenetic trajectories among great apes and humans. J Hum Evol 46: 679-697.
73. Mitteroecker P, Gunz P, Weber GW, Bookstein FL,. 2004b. Regional dissociated heterochrony in multivariate analysis. Ann Anat 186: 463-470.
74. Mitteroecker P, Gunz P, Windhager S, Schaefer K,. 2013. A brief review of shape, form, and allometry in geometric morphometrics, with applications to human facial morphology. Hystrix 24: 59-66.
75. Moss ML., 1973. A functional cranial analysis of primate craniofacial growth. In:, Zingeser M, editor. Fourth international congress of primatologists. Basel: Karger. p 191-208.
76. Moss ML, Salentijn L,. 1971. Differences between the functional matrices in anterior open-bite and in deep overbite. Am J Orthod 60: 264-280.
77. Moss ML, Young RW,. 1960. A functional approach to craniology. Am J Phys Anthropol 18: 281-292.
78. 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. J Hum Evol 59: 555-566.
79. Neubauer S, Gunz P, Hublin JJ,. 2009. The pattern of endocranial ontogenetic shape changes in humans. J Anat 215: 240-255.
80. Nijhout HF,. 2003. The control of growth. Development 130: 5863-5867.
81. Noback ML, Harvati K, Spoor F,. 2011. Climate-related variation of the human nasal cavity. Am J Phys Anthropol 145: 599-614.
82. O'Higgins P, Bastir M, Kupczik K,. 2006. Shaping the human face. Int Congr Series 55-73. p
83. O'Higgins P, Strand Vioarsdõttir U, 1999. New approaches to the quantitative analysis of craniofacial growth and variation. In:, Hoppa R, Fitzgerald C, editors. Human growth in the past: studies from bones and teeth. Cambridge: Cambridge University Press. p 128-160.
84. Oyhenart EE, Orden B, Fucini MC, Mune MC, Pucciarelli HM,. 2003. Sexual dimorphism and postnatal growth of intrauterine growth retarded rats. Growth Dev Aging GDA 67: 73-83.
85. Ponce de Leõn MS, Zollikofer CP,. 2001. Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412: 534-538.
86. Proetz AW,. 1953. Respiratory air currents and their clinical aspects. J Laryngol Otol 67: 1-27.
87. R Development Core Team. 2010. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
88. Rampont M., 1994. Les squelettes, os et dents de foetus, nouveaux-né et enfants du musée anatomique de Strasbourg. Aspect historiques et catalogues. Strasbourg: Université Louis Pasteur Strasbourg.
89. Richtsmeier JT, Corner BD, Grausz HM, Cheverud JM, Danahey SE,. 1993. The role of postnatal growth pattern in the production of facial morphology. Syst Biol 42: 307
90. Rosas A, Bastir M,. 2002. Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex. Am J Phys Anthropol 117: 236-245.
91. Scheuer L, Black SM., 2000. Developmental juvenile osteology. San Diego: Elsevier Academic Press.
92. Shea BT,. 1981. Relative growth of the limbs and trunk in the African apes. Am J Phys Anthropol 56: 179-201.
93. Shea BT,. 1983. Allometry and heterochrony in the african apes. Am J Phys Anthropol 62: 275-289.
94. Stansfield E, Gunz P,. 2011. Skhodnya, khvalynsk, satanay, and podkumok calvariae: possible upper paleolithic hominins from European Russia. J Hum Evol 60: 129-144.
95. Strand Vioarsdõttir U., 1999. Changes in the form of the facial skeleton during growth: a comparative morphometric study of modern humans and Neanderthals. London: University College London.
96. Vioarsdõttir S, Cobb US,. 2004. Inter- and intra-specific variation in the ontogeny of the hominoid facial skeleton: testing assumptions of ontogenetic variability. Ann Anat 186: 423-428.
97. Strand Vioarsdõttir U, O'Higgins P, 2003. Developmental variation in the facial skeleton of anatomically modern Homo sapiens. In:, Thompson J, Krovitz GE, Nelson A, editors. Patterns of growth and development in the genus Homo. Cambridge: Cambridge University Press. p 114-143.
98. Vioarsdõttir S, O'Higgins U, Stringer PC,. 2002. A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton. J Anat 201: 211-229.
99. Stynder DD, Ackermann RR, Sealy JC,. 2007. Craniofacial variation and population continuity during the south african holocene. Am J Phys Anthropol 134: 489-500.
100. Thissen JP, Ketelslegers JM, Underwood LE,. 1994. Nutritional regulation of the insulin-like growth factors. Endocr Rev 15: 80-101.
101. Ubelaker D., 1989. Human skeletal remains. Washington, DC: Taraxacum Press.
102. Ursi WJ, Trotman C-A, McNamara JA Jr, Behrents RG., 1993. Sexual dimorphism in normal craniofacial growth. The Angle Orthodontist 63: 47-56.
103. von Cramon-Taubadel N,. 2014. Evolutionary insights into global patterns of human cranial diversity: population history, climatic and dietary effects. J Anthropol Sci 92: 43-77.
104. Weston EM, Friday AE, Liò P,. 2007. Biometric evidence that sexual selection has shaped the hominin face. PLoS One 2: e710
105. White TD, Black MT, Folkens PA., 2012. Human osteology. Burlington: Academic Press.
106. Wiley DF, Amenta N, Alcantara DA, Deboshmita G, Kil YJ, Delson E, Harcourt-Smith W, Rohlf FJ, St John K, Hamann B., 2005. Evolutionary morphing. In: Proceedings of IEEE visualizations.
107. Williams FL, Godfrey LR, Sutherland MR., 2002. Heterochrony and the evolution of Neandertal and modern human craniofacial form. In:, Minugh-Purvis N, McNamara KJ, editors. Human evolution through developmental change. Baltimore: The John Hopkins University Press. p 405-441.