Relationship of cranial robusticity to cranial form, geography and climate in Homo sapiens

American Journal of Physical Anthropology

Volumn 141, Issue 1, 2010, Pages 97-115

  Baab, Karen L ^a   Freidline, Sarah E ^b,c   Wang, Steven L ^c   Hanson, Timothy ^d  

^a STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cranial morphology; Geometric morphometrics; Human variation

Indexed keywords

AGRICULTURE; ARTICLE; CLIMATE; CLIMATE CHANGE; DIET; FEMALE; GENETIC DISTANCE; GEOGRAPHY; HUMAN; HYPOTHESIS; MALE; MASTICATION; NEUTRAL GENE THEORY; PARTIAL LEAST SQUARES REGRESSION; PHYLOGENY; SKULL;

ADAPTATION, PHYSIOLOGICAL; BODY SIZE; CEPHALOMETRY; CLIMATE; DIET; FEMALE; GEOGRAPHY; HISTORY, ANCIENT; HUMANS; MALE; PRINCIPAL COMPONENT ANALYSIS; SKULL;

CRANIA; HOMO SAPIENS;

EID: 74749090800     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21120     Document Type: Article

References (128)

1. Baab KL. 2007. Cranial shape variation in Homo erectus. Ph.D. dissertation. New York: City University of New York.
2. Banu J, Orhii PB, Okafor MC, Wang L, Kalu DN. 2001. Analysis of the effects of growth hormone, exercise and food restriction on cancellous bone in different bone sites in middle-aged female rats. Mech Ageing Dev 122:849-864.
3. Bernal V, Perez SI, Gonzalez PN. 2006. Variation and causal factors of craniofacial robusticity in Patagonian hunter-gatherers from Late Holocene. Am J Hum Biol 18:748-765.
4. Bilsborough A, Wood BA. 1986. The nature, origin and fate of Homo erectus. In: Wood B, Martin LB, Andrews P, editors. Major topics in primate and human evolution. Cambridge: Cambridge University Press. p 295-316.
5. Boaz NT, Ciochon RL. 2004. Dragon Bone Hill: an ice-age sago of Homo erectus. New York: Oxford University Press.
6. Bookstein FL. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge, England: Cambridge University Press.
7. Bookstein FL, Schaefer K, Prossinger H, Seidler H, Fieder M, Stringer CB, Weber GW, Arsuaga JL, Slice D, Rohlf F, Recheis W, Mariam J, Marcus L. 1999. Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Anat Record 257:217-224.
8. Bräuer G, Mbua E. 1992. Homo erectus features used in cladistics and their variability in Asian and African hominids. J Hum Evol 22:79-108.
9. Bresin A, Kiliaridis S, Strid KG. 1999. Effect of masticatory function on the internal bone structure in the mandible of the growing rat. Eur J Oral Sci 107:35-44.
10. Bridges PS. 1989. Changes in activities with the shift to agriculture in the southeastern United States. Curr Anthropol 30:385-394.
11. Brown P. 1987. Pleistocene homogeneity and Holocene size reduction: the Australian human skeletal evidence. Archaeol Oceania 22:41-71.
12. Brown P. 1994. Cranial vault thickness in Asian Homo erectus and Homo sapiens. Cour Forsch Inst Senckenberg 171:33-46.
13. Bulbeck D. 2001. Robust and gracile Australian crania: the tale of the Willandra Lakes. In: Simanjuntak T, Prasetyo B, Handini R, editors. Sangiran: man, culture and environment in Pleistocene times. Jakarta: Yayasan Obor Indonesia/The National Research Centre of Archaeology/École Française d'Extrême-Orient. p 60-106.
14. Cann HM, Toma C, Cazes L, Legrand M-F, Morel V, Piouffre L, Bodmer J, Bodmer WF, Bonne-Tamir B, Cambon-Thomsen ACZ, Chu J, Carcassi C, Contu L, Du REL, Ferrara GB, Friedlaender JS, Groot H, Gurwitz D, Jenkins T, Herrera RJ, Huang X, Kidd J, Kidd KK, Langaney A, Lin AA, Mehdi SQ, Parham P, Piazza A, Pistillo MP, Qian Y, Shu Q, Xu J, Zhu S, Weber JL, Greely HT, Feldman MW, Thomas G, Dausset J, Cavalli-Sforza LL. 2002. A human genome diversity cell line panel. Science 296:261-262.
15. Carey JW, Steegmann JR. 1981. Human nasal protrusion, latitude, and climate. Am J Phys Anthropol 56:313-319.
16. Carlson DS, van Gerven DP. 1977. Masticatory function and post-Pleistocene evolution in Nubia. Am J Phys Anthropol 46:495-450.
17. Carlson DS, van Gerven DP. 1979. Diffusion, biological determinism, and biocultural adaptation in the Nubian Corridor. Am Anthropol 81:561-580.
18. Carlson KJ, Grine FE, Pearson OM. 2007. Robusticity and sexual dimorphism in the postcranium of modern hunter-gatherers from Australia. Am J Phys Anthropol 134:9-23.
19. Carson EA. 2006a. Maximum-likelihood variance components analysis of heritabilities of cranial nonmetric traits. Hum Biol 78:383-402.
20. Carson EA. 2006b. Maximum likelihood estimation of human craniometric heritabilities. Am J Phys Anthropol 131:169-180.
21. Cattell RB. 1966. The scree test for the number of factors. Multivar Behav Res 1:629-637.
22. Cheverud JM, Buikstra JE. 1981a. Quantitative genetics of skeletal nonmetric traits in the Rhesus macaques on Cayo Santiago. I. Single trait heritabilities. Am J Phys Anthropol 54:43-49.
23. Cheverud JM, Buikstra JE. 1981b. Quantitative genetics of skeletal non-metric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic, genetic, and environmental correlations between traits. Am J Phys Anthropol 54:51-58.
24. Cheverud JM, Buikstra JE. 1982. Quantitative genetics of skeletal non-metric traits in the rhesus macaques on Cayo Santiago. III. Relative heritability of skeletal non-metric and metric traits. Am J Phys Anthropol 59:151-155.
25. Churchill SE. 1998. Cold adaptation, heterochrony, and Neandertals. Evol Anthropol 7:46-61.
26. Ciochon RL, Nisbett RA, Corruccini RS. 1997. Dietary consistency and craniofacial development related to masticatory function in minipigs. J Craniofac Genet Dev Biol 17:96-102.
27. Cónsole GM, Oyhenart EE, Jurado SB, Riccillo FL, Pucciarelli HM, Gómez Dumm CLA. 2001. Effect of undernutrition on cranial components and somatotroph-lactotroph pituitary populations in the squirrel monkey. Cells Tissues Organs 168:272-284.
28. Dieringer D, Schlötterer C. 2003. Microsatellite Analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molec Ecol Notes 3:167-169.
29. Dunsworth HM, Walker A. 2002. Early Genus Homo. In: Hartwig W, editor. The primate fossil record. Cambridge: Cambridge University Press. p 419-426.
30. Endo B. 1966. Experimental studies on the mechanical significance of the form of the human facial skeleton. J Faculty Sci Univ Tokyo (Section V, Anthropol) 3:1-106.
31. Endo B. 1970. Analysis of stress around the orbit due to masseter and temporalis muscles respectively. J Anthropol Soc Nippon 78:251-266.
32. Falconer DS. 1965. The inheritance of liability to certain diseases, estimated from the incidence among relatives. Ann Hum Genet 29:51-76.
33. Falconer DS. 1989. Introduction to quantitative genetics. New York: Wiley.
34. Falconer DS, Mackay TFC. 1996. Introduction to quantitative genetics. Harlow, England: Pearson Education.
35. Forwood MR, Li L, Kelly WL, Bennett MB. 2001. Growth hormone is permissive for skeletal adaptation to mechanical loading. J Bone Miner Res 16:2284-2290.
36. Franciscus RG, Long JC. 1991. Variation in human nasal height and breadth. Am J Phys Anthropol 85:419-427.
37. Frayer DW, Wolpoff MH, Thorne AG, Smith FH, Pope GG. 1993. Theories of modern human origins: the paleontological test. Am Anthropol 95:14-50.
38. Gianola D. 1979. Heritability of polychotomous characters. Genetics 93:1051-1055.
39. Gianola D. 1982. Theory and analysis of threshold characters. J Anim Sci 54:1079-1096.
40. Gilligan I, Bulbeck D. 2007. Environment and morphology in Australian Aborigines: a re-analysis of the Birdsell database. Am J Phys Anthropol 134:75-91.
41. Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW. 1995. An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463-471.
42. González-José R, Ramírez-Rozzi F, Sardi M, Martínez-Abadías N, Hernández M, Pucciarelli HM. 2005. Functional-cranial approach to the influence of economic strategy on skull morphology. Am J Phys Anthropol 128:757-771.
43. Gower JC. 1975. Generalized procrustes analysis. Psychometrika 40:33-51.
44. Greaves WS. 1978. The jaw lever system in ungulates: a new model. J Zool 184:271-285.
45. Gunz P, Harvati K. 2007. The Neanderthal "chignon": variation, integration, and homology. J Hum Evol 52:262-274.
46. Halverson MS, Bolnick DA. 2008. An ancient DNA test of a founder effect in Native American ABO blood group frequencies. Am J Phys Anthropol 137:342-347.
47. Hanihara T. 1996. Comparison of craniofacial features of major human groups. Am J Phys Anthropol 99:389-412.
48. Hanson TE, Pearson OM. 2007. Fitting Manova models with missing continuous or ordinal data using reference priors. Commun Stat Simulat 36:621-630.
49. Harvati K. 2003. The Neanderthal taxonomic position: models of intra-and inter-specific craniofacial variation. J Hum Evol 44:107-132.
50. Harvati K, Weaver TD. 2006a. Human cranial anatomy and the differential preservation of population history and climate signatures. Anat Rec A 288:1225-1233.
51. Harvati K, Weaver TD. 2006b. Reliability of cranial morphology in reconstructing Neanderthal phylogeny. In: Harvati K, Harrison T, editors. Neanderthals revisited: new approaches and perspectives. Dordrecht: Springer. p 239-254.
52. Hennessy RJ, Stringer CB. 2002. Geometric morphometric study of the regional variation of modern human craniofacial form. Am J Phys Anthropol 117:37-48.
53. Hernández M, Lalueza C, García-Moro C. 1997. Fueguian cranial morphology: the adaptation to a cold, harsh environment. Am J Phys Anthropol 103:103-117.
54. Hilloowala RA, Trent RB. 1987. Supraorbital ridge and masticatory apparatus II: Humans (Eskimos). Hum Evol 3:351-356.
55. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70.
56. Hood GM. 2008. PopTools version 3.0.2. Available on the internet URL at: http://www.cse.csiro.au/poptools.
57. Howells WW. 1973. Cranial variation in man. Pap Peabody Mus Am Archaeol Ethnol 67:1-259.
58. Howells WW. 1989. Skull shapes and the map: craniometric analyses in the dispersion of modern Homo. Pap Peabody Mus Am Archaeol Ethnol 79:1-189.
59. Hrdlička A. 1910. Contribution to the anthropology of central and Smith Sound Eskimo. Anthrop Pap AmMus nat Hist 5:177-280.
60. Hublin J-J. 1986. Some comments on the diagnostic features of Homo erectus. Anthropos (Brno) 23:175-187.
61. Hylander WL, Picq PG, Johnson KR. 1991. Masticatory-stress hypothese and the supraorbital region of primates. Am J Phys Anthropol 86:1-36.
62. Kaiser HF. 1961. A note on Guttman's lower bound for the number of common factors. Br J Psychol 14:1-2.
63. Kelly RL. 1995. The foraging spectrum: diversity in huntergatherer lifeways. Washington, DC: Smithsonian Institution Press.
64. Klingenberg CP. 2008. MorphoJ: faculty of life sciences, University of Manchester, UK. Available at: http://www.flywings.org.uk/MorphoJ-page.htm.
65. Konigsberg LW. 2000. Quantitative variation and genetics. In: Stinson S, Bogin B, Huss-Ashmore R, O'Rourke D, editors. Human biology: an evolutionary and biocultural approach. New York: Wiley. p 135-162.
66. Konigsberg LW, Kohn LAP, Cheverud JM. 1993. Cranial deformation and nonmetric trait variation. Am J Phys Anthropol 90:35-48.
67. Krzanowski WJ. 2000. Principles of multivariate analysis: a user's perspective. Oxford: Oxford University Press.
68. Lahr MM. 1995. Patterns of modern human diversification: implications for Amerindian origins. Yearb Phys Anthropol 38:163-198.
69. Lahr MM. 1996. The evolution of modern human diversity. Cambridge: Cambridge University Press.
70. Lahr MM, Wright RSV. 1996. The question of robusticity and the relationship between cranial size and shape in Homo sapiens. J Hum Evol 31:157-191.
71. Lalueza C, Hernández M, García-Moro C. 1997. La morfología facial de las poblaciones fueguinas: ¿reflejo de una adaptación al frío? An Inst Patagon Ser Cs Hum 25:45-58.
72. Lande R. 1992. Neutral theory of quantitative genetic variance in an island model with local extinction and colonization. Evolution 46:381-389.
73. Larsen CS. 1981. Skeletal and dental adaptations to the shift to agriculture on the Georgia Coast. Curr Anthropol 22:422-423.
74. Larsen CS. 1982. The anthropology of St. Catherines Island. 3, Prehistoric human biological adaptation. Anthrop Pap Am Mus Nat Hist 57:157-270.
75. Larsen CS. 1984. Health and disease in prehistoric Georgia: the transition to agriculture. In: Cohen MN, Armelagos GJ, editors. Paleopathology at the origins of agriculture. Orlando, FL: Academic Press. p 367-392.
76. Larsen CS. 1995. Biological changes in human populations with agriculture. Ann Rev Anthropol 24:185-213.
77. Larsen CS. 1997. Bioarchaeology: interpreting behavior from the human skeleton. Cambridge: Cambridge University Press.
78. Larsen CS, Ruff CB. 1994. The stresses of conquest in Spanish Florida: structural adaptation and change before and after contact. In: Larsen CS, Milner GR, editors. In the wake of contact: biological responses to conquest. New York: Wiley-Liss. p 21-34.
79. Leonard WR, Sorensen MV, Galloway VA, Spencer GJ, Mosher MJ. 2002. Climatic influences on basal metabolic rates among circumpolar populations. Am J Hum Biol 14:609-620.
80. Leigh SR, Relethford JH, Park PB, Konigsberg LW. 2003. Morphological differentiation of Gorilla subspecies. In: Taylor AB, Goldsmith ML, editors. Gorilla biology: a multidisciplinary perspective. Cambridge: Cambridge University Press. p 104-131.
81. Lieberman DE. 1996. How and why humans grow thin skulls: experimental evidence for systemic cortical robusticity. Am J Phys Anthropol 101:217-236.
82. Lieberman DE, Krovitz GE, Yates FW, Devlin M, St. Claire M. 2004. Effects of food processing on masticatory strain and craniofacial growth in a retrognathic face. J Hum Evol 46:655-677.
83. López-Fanjul C, Fernández A, Toro MA. 2003. The effect of neutral nonadditive gene action on the quantitative index of population divergence. Genetics 164:1627-1633.
84. Lynch M, Walsh JB. 1998. Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
85. Mantel N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res 27:209-220.
86. Mardia KV, Bookstein FL, Moreton IJ. 2000. Statistical assessment of bilateral symmetry of shapes. Biometrika 87:285-300.
87. McNulty KP. 2003. Geometric morphometric analyses of extant and fossil hominoid craniofacial morphology, Ph.D. dissertation. New York: City University of New York.
88. Mulligan CJ, Hunley K, Cole S, Long JC. 2004. Population genetics, history, and health patterns in Native Americans. Annu Rev Genomics Hum Genet 5:295-315.
89. New M, Hulme M, Jones P. 1999. Representing twentieth-century space-time climate variability: I, development of a 1961-90 mean monthly terrestrial climatology. J Clim 12:829-856.
90. New M, Hulme M, Jones P. 2000. Representing twentieth-century space-time climate variability. part II: development of 1901-96 monthly grids of terrestrial surface climate. J Clim 13:2217-2238.
91. Perez SI, Bernal V, Gonzalez PN. 2007. Morphological differentiation of aboriginal human populations from Tierra del Fuego (Patagonia): implications for South American peopling. Am J Phys Anthropol 133:1067-1079.
92. Perzigian AJ, Tench PA, Braun DJ. 1984. Prehistoric health in the Ohio River Valley. In: Cohen MN, Armelagos GJ, editors. Paleopathology at the origins of agriculture London. London: Academic Press. p 347-366.
93. Ramachandran S, Deshpande O, Roseman CC, Rosenberg NA, Feldman MW. 2005. Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102:15942-15947.
94. Ravosa MJ. 1991. Interspecific perspecitve on mechanical and nonmechanical models of primate circumorbital morphology. Am J Phys Anthropol 86:369-396.
95. Rightmire GP. 1990. The evolution of Homo erectus: comparative anatomical studies of an extinct human species. New York: Cambridge University Press.
96. Rohlf FJ. 1999. Shape statistics: procrustes superimpositions and tangent spaces. J Classif 16:197-223.
97. Rohlf FJ, Corti M. 2000. Use of two-block partial least-squares to study covariation in shape. Syst Biol 49:740-753.
98. Rohlf FJ, Slice D. 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40-59.
99. Roseman CC. 2004. Detecting inter-regionally diversifying natural selection on modern human cranial form using matched molecular and morphometric data. Proc Natl Acad Sci USA 101:12824-12829.
100. Roseman CC, Weaver TD. 2004. Multivariate apportionment of global human craniometric diversity. Am J Phys Anthropol 125:257-263.
101. Rosenberg NA, Mahajan S, Ramachandran S, Zhao C, Pritchard JK, Feldman MW. 2005. Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genet 1:e1-e70.
102. Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW. 2002. Genetic structure of human populations. Science 298:2381-2385.
103. Ross CF, Hylander WL. 1996. In vivo and in vitro bone strain analysis of the circumorbital region of Aotus and the function of the postorbital septum. Am J Phys Anthropol 101:183-215.
104. Russell MD. 1985. The supraobital torus: a most remarkable peculiarity. Curr Anthropol 26:337-350.
105. Sardi ML, Novellino PS, Pucciarelli HM. 2006. Craniofacial morphology in the Argentine Center-West: consequences of the transition to food production. Am J Phys Anthropol 130: 330-343.
106. Schwartz JH. 2004. Getting to know Homo erectus. Science 305:53-54.
107. Singleton M. 2005. Geometric morphometric analysis of functional divergence of mangabey facial form. J Anthropol Sci 82:29-45.
108. Slice DE. 1998. Morpheus et al.: software for morphometric research. Department of Ecology and Evolution (Stony Brook, New York): State University of New York.
109. Smith HF, Terhune CE, Lockwood CA. 2007. Genetic, geographic, and environmental correlates of human temporal bone variation. Am J Phys Anthropol 134:312-322.
110. Smouse PE, Long JC, Sokal RT. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627-632.
111. Spencer MA. 1998. Force production in the primate masticatory system-electromyographic tests of biomechanical hypotheses. J Hum Evol 34:25-54.
112. Spencer MA. 1999. Constraints on masticatory system evolution in anthropoid primates. Am J Phys Anthropol 108:483-506.
113. Spencer MA, Demes B. 1993. Biomechanical analysis of masticatory system configuration in Neandertals and Inuits. Am J Phys Anthropol 91:1-20.
114. Spencer MA, Ungar PS. 2000. Craniofacial morphology, diet and incisor use in three Native American populations. Int J Osteoarchaeol 10:229-241.
115. Strand Viodarsdóttir U, O'Higgins P, Stringer CB. 2002. A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton J Anat 201:211-229.
116. Stringer CB. 1984. The definition of Homo erectus and the existence of the species in Africa and Europe. Cour Forsch Inst Senckenberg 69:131-143.
117. Villmoare B. 2005. Metric and non-metric randomization methods, geographic variation, and the single-species hypothesis for Asian and African Homo erectus. J Hum Evol 49:680-701.
118. Vogl C, Atchley WC, Cowley DE, Crenshaw P, Murray JD, Pomp D. 1993. The epigenetic influence of growth hormone on skeletal development. Growth Dev Aging 57:163-182.
119. Walker PL. 2008. Sexing skulls using discriminant function analysis of visually assessed traits. Am J Phys Anthropol 136: 39-50.
120. Wang S, Lewis CM Jr, Jakobsson M, Ramachandran S, Ray N, Bedoya G, Rojas W, Parra MV, Molina JA, Gallo C, Mazzotti G, Poletti G, Hill K, Hurtado AM, Labuda D, Klitz W, Barrantes R, Bortolini MC, Salzano FM, Petzl-Erler ML, Tsuneto LT, Llop E, Rothhammer F, Excoffier L, Feldman MW, Rosenberg NA, Ruiz-Linares A. 2007. Genetic variation and population structure in Native Americans. PLoS Genet 3:e185.
121. Weaver TD, Roseman CC, Stringer CB. 2007. Were Neanderthal and modern human cranial differences produced by natural selection or genetic drift? J Hum Evol 53:135-145.
122. Wolpoff MH. 1985. On explaining the supraorbital torus. Curr Anthropol 26:522.
123. Wolpoff MH. 1999. Paleoanthropology. Boston: McGraw-Hill.
124. Wolpoff MH, Wu XZ, Thorne AG. 1984. Modern Homo sapiens origins: a general theory of hominid evolution involving the fossil evidence from East Asia. In: Smith FH, and Spencer F, editors. The origins of modern humans. New York: Alan R. Liss. p 411-484.
125. Wood BA, Richmond BG. 2000. Human evolution: taxonomy and paleobiology. J Anat 197:19-60.
126. Wright S. 1934. An analysis of variability in number of digits in an inbred strain of guinea pigs. Genetics 19:506-536.
127. y'Edynak G, Fleisch S. 1983. Microevolution and biological adaptability in the transition from food-collecting to foodproducing in the Iron Gates of Yugoslavia. J Hum Evol 12:279-296.
128. Zelditch M, Swiderski D, Sheets DH, Fink W. 2004. Geometric morphometrics for biologists: a primer. New York: Elsevier Academic Press.