Global Geometric Morphometric Analyses of the Human Pelvis Reveal Substantial Neutral Population History Effects, Even across Sexes

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Betti, Lia ^a,b   von Cramon Taubadel, Noreen ^a   Manica, Andrea ^b   Lycett, Stephen J ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANALOG DIGITAL CONVERTER; ANATOMIC LANDMARK; ANATOMIC MODEL; ANATOMICAL VARIATION; ARTICLE; BODY SIZE; COMPARATIVE ANATOMY; CONTROLLED STUDY; FEMALE; GEOGRAPHIC DISTRIBUTION; GEOGRAPHIC ORIGIN; HIP; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MATHEMATICAL COMPUTING; MORPHOMETRICS; PELVIC GIRDLE; PELVIS; PHENOTYPIC VARIATION; POPULATION RESEARCH; SEX DETERMINATION; SEX DIFFERENCE;

BIOLOGICAL EVOLUTION; FEMALE; FOUNDER EFFECT; GENETICS, POPULATION; HUMANS; MALE; MODELS, THEORETICAL; PELVIS; PHENOTYPE; SELECTION, GENETIC; SEX CHARACTERISTICS;

EID: 84873585922     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055909     Document Type: Article

References (104)

1. Roseman CC, Weaver TD, (2007) Molecules versus morphology? Not for the human cranium. BioEssays 29: 1185-1188.
2. Relethford JH, (1994) Craniometric variation among modern human populations. Am J Phys Anthropol 95: 53-62.
3. Relethford JH, (2002) Apportionment of global human genetic diversity based on craniometrics and skin color. Am J Phys Anthropol 118: 393-398.
4. Relethford JH, (2004b) Global patterns of isolation by distance based on genetic and morphological data. Hum Biol 76: 499-513.
5. González-José R, Van der Molen S, González-Pérez E, Hernández M, (2004) Patterns of phenotypic covariation and correlation in modern humans as viewed from morphological integration. Am J Phys Anthropol 123: 69-77.
6. Roseman CC, (2004) Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data. Proc Natl Acad Sci U S A 101: 12824-12829.
7. Roseman CC, Weaver TD, (2004) Multivariate apportionment of global human craniometric diversity. Am J Phys Anthropol 125: 257-263.
8. Harvati K, Weaver TD, (2006a) Human cranial anatomy and the differential preservation of population history and climate signatures. Anat Rec A 288: 1225-1233.
9. 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 Netherlands. 239-254.
10. Manica A, Amos W, Balloux F, Hanihara T, (2007) The effect of ancient population bottlenecks on human phenotypic variation. Nature 448: 346-349.
11. Hanihara T, (2008) Morphological variation of major human populations based on nonmetric dental traits. Am J Phys Anthropol 136: 169-182.
12. Betti L, Balloux F, Hanihara T, Manica A, (2009) Ancient demography, not climate, explains within-population phenotypic diversity in humans. Proc Royal Soc, B 276: 809-814.
13. Smith HF, (2009) Which cranial regions reflect molecular distances reliably in humans? Evidence from three-dimensional morphology. Am J Hum Biol 21: 36-47.
14. von Cramon-Taubadel N, (2009a) Congruence of individual cranial bone morphology and neutral molecular affinity patterns in modern humans. Am J Phys Anthropol 140: 205-215.
15. von Cramon-Taubadel N, Weaver TD, (2009) Insights from a quantitative genetic approach to human morphological evolution. Evol Anthropol 18: 237-240.
16. Lewontin R, (1972) The apportionment of human diversity. Evol Biol 6: 381-398.
17. Barbujani G, Magagni A, Minch E, Cavalli-Sforza LL, (1997) An apportionment of human DNA diversity. Proc Natl Acad Sci U S A 94: 4516-4519.
18. Jorde LB, Watkins WS, Bamshad MJ, Dixon ME, Ricker CE, et al. (2000) The distribution of human genetic diversity: A comparison of mitochondrial, autosomal, and Y-chromosome data. Am J Hum Genet 66: 979-988.
19. Long JC, (2009) Update to Long and Kittles's "Human genetic diversity and the nonexistence of biological races" (2003): Fixation on an index. Hum Biol 81: 799-803.
20. Long JC, Kittles RA, (2003) Human genetic diversity and the nonexistence of biological races. Hum Biol 75: 449-471.
21. Edwards AWF, (2003) Human genetic diversity: Lewontin's fallacy. BioEssays 25: 798-801.
22. von Cramon-Taubadel N, (2009b) Revisiting the homoiology hypothesis: the impact of phenotypic plasticity on the reconstruction of human population history from craniometric data. J Hum Evol 57: 179-190.
23. von Cramon-Taubadel N, (2011b) The relative efficacy of functional and developmental cranial modules for reconstructing global human population history. Am J Phys Anthropol 146: 83-93.
24. Cavalli-Sforza LL, Menozzi P, Piazza A (1994). The history and geography of human genes. Princeton: Princeton University Press.
25. Eller E, (1999) Population substructure and isolation by distance in three continental regions. Am J Phys Anthropol 108: 147-159.
26. Betti L, Balloux F, Hanihara T, Manica A, (2010) The relative role of drift and selection in shaping the human skull. Am J Phys Anthropol 141: 76-82.
27. Prugnolle F, Manica A, Balloux F, (2005) Geography predicts neutral genetic diversity of human populations. Curr Biol 15: R159-160.
28. Ramachandran S, Deshpande O, Roseman CC, Rosenberg NA, Feldman MW, et al. (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 U S A 102: 15942-15947.
29. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319: 1100-1104.
30. von Cramon-Taubadel N, Lycett SJ, (2008) Human cranial variation fits iterative founder effect model with African origin. Am J Phys Anthropol 136: 108-113.
31. Betti L, von Cramon-Taubadel N, Lycett SJ, (2012) Human pelvis and long bones reveal differential preservation of ancient population history and migration out of Africa. Hum Biol 84: 139-152.
32. Ruff CB, (1993) Climatic adaptation and hominid evolution: The thermoregulatory imperative. Evol Anthropol 2: 53-60.
33. Ruff CB, (1994) Morphological adaptation to climate in modern and fossil hominids. Am J Phys Anthropol 37: 65-107.
34. Holliday TW, (1997a) Body proportions in Late Pleistocene Europe and modern human origins. J Hum Evol 32: 423-447.
35. Holliday TW, (1997b) Postcranial evidence of cold adaptation in European Neandertals. Am J Phys Anthropol 104: 245-258.
36. Stock J, Pfeiffer S, (2001) Linking structural variability in long bone diaphyses to habitual behaviors: Foragers from the southern African Later Stone Age and the Andaman Islands. Am J Phys Anthropol 115: 337-348.
37. Stock JT, (2006) Hunter-gatherer postcranial robusticity relative to patterns of mobility, climatic adaptation, and selection for tissue economy. Am J Phys Anthropol 131: 194-204.
38. Holliday TW, Hilton CE, (2010) Body proportions of circumpolar peoples as evidenced from skeletal data: Ipiutak and Tigara (Point Hope) versus Kodiak Island Inuit. Am J Phys Anthropol 142: 287-302.
39. Waterman HC, (1929) Studies in the evolution of the pelvis of man and other primates. Bull Am Mus Nat Hist 58: 585-642.
40. Reynolds ED, (1931) The evolution of the human pelvis in relation to the mechanics in the erect posture. Pap Peabody Mus 9: 255-334.
41. Schultz AH, (1936) Characters common to higher primates and characters specific for man (continued). Q Rev Biol 11: 425-455.
42. McHenry HM, Corruccini RS, (1978) Analysis of the hominoid os coxae by Cartesian coordinates. Am J Phys Anthropol 48: 215-226.
43. Steudel K, (1978) A multivariate analysis of the pelvis of early hominids. J Hum Evol 7: 583-595.
44. Berge C, (1984) Multivariate analysis of the pelvis for hominids and other extant primates: Implications for the locomotion and systematics of the different species of australopithecines. J Hum Evol 13: 555-562.
45. Lovejoy CO, (1988) Evolution of human walking. Sci Am 259: 118-125.
46. Tague RG, (1992) Sexual dimorphism in the human bony pelvis, with a consideration of the Neandertal pelvis from Kebara Cave, Israel. Am J Phys Anthropol 88: 1-21.
47. Ward CV, (2002) Interpreting the posture and locomotion of Australopithecus afarensis: Where do we stand?. Am J Phys Anthropol 119: 185-215.
48. Weaver TD, Hublin JJ, (2009) Neandertal birth canal shape and the evolution of human childbirth. Proc Natl Acad Sci U S A 106: 8151-8156.
49. DeSilva JM, (2011) A shift toward birthing relatively large infants early in human evolution. Proc Natl Acad Sci U S A 108: 1022-1027.
50. Thoms H, Foote WR, Friedman I, (1939) The clinical significance of pelvic variations: A dimensional study of the upper, mid, and lower pelvis in 200 white primiparous women. Am J Obstet Gynecol 38: 634-642.
51. Tague RG, (1989) Variation in pelvic size between males and females. Am J Phys Anthropol 80: 59-71.
52. Rosenberg KR, (1992) The evolution of modern human childbirth. Am J Phys Anthropol 35: 89-124.
53. Ruff C, (2002) Variation in human body size and shape. Annu Rev Anthropol 31: 211-232.
54. Cox M, Scott A, (1992) Evaluation of the obstetric significance of some pelvic characters in an 18th century British sample of known parity status. Am J Phys Anthropol 89: 431-440.
55. Correia H, Balseiro S, De Areia M, (2005) Sexual dimorphism in the human pelvis: Testing a new hypothesis. HOMO 56: 153-160.
56. Kurki HK, (2011) Pelvic dimorphism in relation to body size and body size dimorphism in humans. J Hum Evol 61: 631-643.
57. Krogman WM, (1951) The role of physical anthropology in dental and medical research. Am J Phys Anthropol 9: 211-218.
58. Washburn SN, (1960) Tools and human evolution. Sci Am 203: 3-15.
59. Rosenberg K, Trevathan W, (1995) Bipedalism and human birth: The obstetrical dilemma revisited. Evol Anthropol 4: 161-168.
60. Weaver TD (2002). A multi-causal functional analysis of hominid hip morphology. Palo Alto: Stanford University. Unpublished PhD Thesis.
61. Ruff CB, (1991) Climate and body shape in hominid evolution. J Hum Evol 21: 81-105.
62. Ruff C, (2010) Body size and body shape in early hominins- implications of the Gona Pelvis. J Hum Evol 58: 166-178.
63. Bergmann C, (1847) Uber die verhaltniesse der warmeokonomie der thiere zu ihrer grosse. Gotteningen Studien 1: 595-708.
64. Tague RG, (1995) Variation in pelvic size between males and females in nonhuman anthropoids. Am J Phys Anthropol 97: 213-233.
65. Kurki HK, (2007) Protection of obstetric dimensions in a small-bodied human sample. Am J Phys Anthropol 133: 1152-1165.
66. Aiello LC, Dean C (1990). An introduction to human evolutionary anatomy. London: Academic Press.
67. Phenice TW, (1969) A newly developed visual method of sexing the os pubis. Am J Phys Anthropol 30: 297-301.
68. Işcan MY, Derrick K, (1984) Determination of sex from sacroiliac joint: A visual assessment technique. Florida Scientist 47: 94-98.
69. Sutherland LD, Suchey JM, (1991) Use of the ventral arc in pubic sex determination. J Forensic Sci 36: 501-511.
70. von Cramon-Taubadel N, Frazier BC, Lahr MM, (2007) The problem of assessing landmark error in geometric morphometrics: Theory, methods, and modifications Am J Phys Anthropol. 134: 24-35.
71. Rohlf FJ, (1990) Morphometrics. Annu Rev Ecol Syst 21: 299-316.
72. Rohlf FJ, Slice D, (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Biol 39: 40-59.
73. Rohlf FJ, Marcus LF, (1993) A revolution in morphometrics. Trends Ecol Evol 8: 129-132.
74. Slice DE (1996). Three-dimensional generalized resistance fitting and the comparison of least-squares and resistant fit residuals. In: Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE, editors. Advances in morphometrics. New York: Plenum Press. 179-199.
75. O'Higgins P, Jones N, (1998) Facial growth in Cercocebus torquatus: an application of three-dimensional geometric morphometric techniques to the study of morphological variation. J Anat 193: 251-272.
76. R Development Core Team (2011). R: A language and environment for statistical computing. Version 2.14. Vienna: R Foundation for Statistical Computing.
77. Relethford JH, Crawford MH, Blangero J, (1997) Genetic drift and gene flow in post-famine Ireland. Hum Biol 69: 443-465.
78. Harpending H, Jenkins T (1973). Genetic distance among Southern African populations. In: Crawford MH, Workman PL, editors. Methods and theories of anthropological genetics. Albuquerque: University of New Mexico Press. 177-199.
79. Relethford JH, Blangero J, (1990) Detection of differential gene flow from patterns of quantitative variation. Hum Biol 62: 5-25.
80. Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004). Geometric Morphometrics for Biologists: A Primer. London: Elsevier Academic Press.
81. Franklin D, Cardini A, Oxnard CE, (2010) A geometric morphometric approach to the quantification of population variation in sub-Saharan African crania. Am J Hum Biol 22: 23-35.
82. Manica A, Prugnolle F, Balloux F, (2005) Geography is a better determinant of human genetic differentiation than ethnicity. Hum Genet 118: 366-371.
83. Akaike H (1973). Information theory and an extension of the maximum likelihood principle In: Petrov BN, Csaki F, editors. Second international Symposium on Information theory. Budapest: Academiai Kiado. 267-281.
84. Latter BDH, (1980) Genetic differences within and between populations of the major human subgroups. Am Nat 116: 220-237.
85. Ryman N, Chakraborty R, Nei M, (1983) Differences in the relative distribution of human gene diversity between electrophoretic and red and white cell antigen loci. Hum Hered 33: 93-102.
86. Jablonski NG, Chaplin G, (2000) The evolution of human skin coloration. J Hum Evol 39: 57-106.
87. Currey J, (1984) Comparative mechanical properties and histology of bone. Am Zool 24: 5-12.
88. Lieberman DE, (1996) How and why humans grow thin skulls: Experimental evidence for systemic cortical robusticity. Am J Phys Anthropol 101: 217-236.
89. Walker PL, (2005) Greater sciatic notch morphology: Sex, age, and population differences. Am J Phys Anthropol 127: 385-391.
90. Dunsworth HM, Warrener AG, Deacon T, Ellison PT, Pontzer H, (2012) Metabolic hypothesis for human altriciality. Proc Natl Acad Sci U S A 109: 15212-15216.
91. Wells JCK, DeSilva JM, Stock JT, (2012) The obstetric dilemma: an ancient game of Russian roulette, or a variable dilemma sensitive to ecology? Yearb Phys Anthropol 55: 40-71.
92. Smith HF, (2011) The role of genetic drift in shaping modern human cranial evolution: A test using microevolutionary modeling. Int J Evol Biol 2011: 145262.
93. von Cramon-Taubadel N, (2011a) Global human mandibular variation reflects differences in agricultural and hunter-gatherer subsistence strategies. Proc Natl Acad Sci U S A 108: 19546-19551.
94. Relethford JH, (2004a) Boas and beyond: Migration and craniometric variation. Am J Hum Biol 16: 379-386.
95. Weaver TD, Roseman CC, Stringer CB, (2007) Were Neandertal and modern human cranial differences produced by natural selection or genetic drift? J Hum Evol 53: 135-145.
96. Weaver TD, Roseman CC, Stringer CB, (2008) Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans. Proc Natl Acad Sci U S A 105: 4645-4649.
97. Relethford JH, (2010) Population-specific deviations of global human craniometric variation from a neutral model. Am J Phys Anthropol 142: 105-111.
98. Pinhasi R, von Cramon-Taubadel N, (2009) Craniometric data supports demic diffusion model for the spread of agriculture into Europe. PLoS ONE 4: e6747.
99. von Cramon-Taubadel N, Pinhasi R, (2011) Craniometric data support a mosaic model of demic and cultural Neolithic diffusion to outlying regions of Europe. Proc Royal Soc, B 278: 2874-2880.
100. Hubbe M, Harvati K, Neves W, (2011) Paleoamerican morphology in the context of European and East Asian late Pleistocene variation: Implications for human dispersion into the new world. Am J Phys Anthropol 144: 442-453.
101. Hubbe M, Neves WA, Harvati K, (2010) Testing evolutionary and dispersion scenarios for the settlement of the New World. PLoS ONE 5: e11105.
102. de Azevedo S, Nocera A, Paschetta C, Castillo L, González M, et al. (2011) Evaluating microevolutionary models for the early settlement of the New World: The importance of recurrent gene flow with Asia. Am J Phys Anthropol 146: 539-552.
103. Devor EJ, (1987) Transmission of human craniofacial dimensions. J Craniofac Genet Dev Biol 7: 95-106.
104. Williams-Blangero S, Blangero J, (1992) Quantitative genetic analysis of skin reflectance: a multivariate approach. Hum Biol 64: 35-49.