Sexual dimorphism in multiple aspects of 3D facial symmetry and asymmetry defined by spatially dense geometric morphometrics

Journal of Anatomy

Volumn 221, Issue 2, 2012, Pages 97-114

  Claes, Peter ^a,b   Walters, Mark ^d   Shriver, Mark D ^e   Puts, David ^e   Gibson, Greg ^f   Clement, John ^b   Baynam, Gareth ^g   Verbeke, Geert ^c   Vandermeulen, Dirk ^a   Suetens, Paul ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c KU LEUVEN   (Belgium)

^d PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

^f GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^g UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

3D faces; Geometric morphometrics; Permutational statistics; Sexual dimorphism; Spatially dense; Symmetry and asymmetry

Indexed keywords

ANALYSIS OF VARIANCE; ANTHROPOMETRIC PARAMETERS; ARTICLE; CHEEK; CHIN; COVARIANCE; DEVELOPMENTAL BIOLOGY; FACE ASYMMETRY; FACE SYMMETRY; FEMALE; FOREHEAD; GENETICS; HUMAN; MALE; MORPHOMETRICS; MOUTH; NOSE; PRIORITY JOURNAL; SEX DIFFERENCE; SKULL; SOFT TISSUE; TISSUE GROWTH; VARIANCE;

ADULT; ANALYSIS OF VARIANCE; ANTHROPOMETRY; FACE; FACIAL ASYMMETRY; FEMALE; HUMANS; MALE; SEX CHARACTERISTICS; SEX FACTORS; YOUNG ADULT;

EID: 84863519637     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2012.01528.x     Document Type: Article

References (108)

1. Ackermann RR, Cheverud JM (2000) Phenotypic covariance structure in tamarins (Genus Saguinys): a comparison of variation patterns using matrix correlation and common principal component analysis. Am J Phys Anthropol 111, 489-501.
2. Adams D (2011) Re: tribulations with permutations. In Morphmet, available at http://www.mail-archive.com/morphmet@morphometrics.org/msg02265.html.
3. Adams DC, Rohlf F, Slice D (2004) Geometric morphometrics: ten years of progress following the revolution. Ital J Zool 71, 5-16.
4. Aeria G, Claes P, Vandermeulen D, et al. (2010) Targeting specific facial variation for different identification tasks. Forensic Sci Int 201, 118-124.
5. Anderson JM (2001a) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58, 626-639.
6. Anderson MJ (2001b) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26, 32-46.
7. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245-253.
8. Anderson MJ, Millar RB (2004) Spatial variation and effects of habitat on temperate reef fish assemblages in northeastern New Zealand. J Exp Mar Biol Ecol 305, 191-221.
9. Andresen PR, Bookstein FL, Conradsen K, et al. (2000) Surface-bounded growth modeling applied to human mandibles. IEEE Trans Med Imaging 19, 1053-1063.
10. Badyaev AV, Hill GE (2000) The evolution of sexual dimorphism in the House Finch. I. Population divergence in morphological covariance structure. Evolution 54, 1784-1794.
11. Badyaev A, Hill GE, Stoehr AM, et al. (2000) The evolution of sexual size dimorphism in the House Finch. II. Population divergence in relation to local selection. Evolution 54, 2134-2144.
12. 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.
13. Baudouin JY, Tiberghien G (2004) Symmetry, averagness, and feature size in the facial attractiveness of women. Acta Psychol (Amst) 117, 313-332.
14. Baynam G, Claes P, Craig JM, et al. (2011) Intersections of epigenetics, twinning and developmental asymmetries: insights into monogenic and complex diseases and role for 3D facial analysis. Twin Res Hum Genet 14, 305-315.
15. Baynam G, Walters M, Claes P, et al. (2012) 3D facial analysis can investigate vaccine responses. Med Hypotheses 78, 497-501.
16. Bigoni L, Velemínska J, Brůžek J (2010) Three-dimensional geometric morphometrics analysis of cranio-facial sexual dimorphism in a Central European sample of known sex. J Comp Hum Biol 61, 16-32.
17. Bock MT, Bowman AW (2006) On the measurement and analysis of asymmetry with applications to facial modelling. Appl Stat 55, 77-91.
18. Bookstein FL (1997a) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med Image Anal 1, 225-243.
19. Bookstein FL (1997b) Shape and the information in medical images: a decade of the morphometric synthesis. Comput Vis Image Underst 66, 97-118.
20. Box GEP (1949) A general distribution theory for a class of likelihood criteria. Biometrika 36, 317-346.
21. Brombin C, Salmaso L (2009) Multi-aspect permutation tests in shape analysis with small sample size. Comput Stat Data Anal 53, 3921-3931.
22. Bugaighis I, O'Higgens P, Tiddeman B, et al. (2010) Three-dimensional geometric morphometrics applied to the study of children with cleft lip and/or palate from the North East of England. Eur J Orthod 32, 514-521.
23. Burris RP, Roberts SC, Welling LLM, et al. (2011) Heterosexual romantic couples mate assortatively for facial symmetry, but not masculinity. Pers Soc Psychol Bull 37, 601-613.
24. Claes P (2007) A robust statistical surface registration framework using implicit function representations: application in craniofacial reconstruction. In: Faculteit ingenieurswetenschappen, department Elektrotechniek, afdeling PSI, Thesis. Leuven: K.U.Leuven. Available at
25. Claes P, Vandermeulen D, De Greef S, et al. (2006) Craniofacial reconstruction using a combined statistical model of face shape and soft tissue depths: methodology and validation. Forensic Sci Int 159, 147-158.
26. Claes P, Vandermeulen D, De Greef S, et al. (2010a) Bayesian estimation of optimal craniofacial reconstructions. Forensic Sci Int 201, 146-152.
27. Claes P, Vandermeulen D, De Greef S, et al. (2010b) Computerized craniofacial reconstruction: conceptual framework and review. Forensic Sci Int 201, 138-145.
28. Claes P, Walters M, Vandermeulen D, et al. (2011) Spatially-dense 3D facial asymmetry assessment in both typical and disordered growth. J Anat 219, 444-455.
29. Claes P, Walters M, Clement JG (2012a) Improved facial outcome assessment using a 3D anthropometric mask. Int J Oral Maxillofac Surg 41, 324-330.
30. Claes P, Daniels K, Walters M, et al. (2012b) Dysmorphometrics: the modelling of morphological abnormalities. Theor Biol Med Model 9, 1-39.
31. Corsten LCA, Van Eijnsbergen CA (1972) Multiplicative effects in a two-way analysis of variance. Stat Neerl 26, 61-68.
32. Deleon VB (2007) Fluctuating asymmetry and stress in a medieval nubian population. Am J Phys Anthropol 132, 520-534.
33. Dias C, Krzanowski WJ (2006) Choosing components in the additive main effect and multiplicative interaction (AMMI) models. Scientia Agricola 63, 169-175.
34. Dryden IL, Mardia KV (1998) Statistical Shape Analysis. New York: John Wiley & Sons.
35. Enlow DH (1968) The human face: an account of the postnatal growth and development of the craniofacial skeleton. Science 162, 1470.
36. Enlow DH, Hans MM (1996) Essential of Facial Growth. Philadelphia: Saunders.
37. Ercan I, Ozdemir ST, Etoz A, et al. (2008) Facial asymmetry in young healty subjects evaluated by statistical shape analysis. J Anat 213, 663-669.
38. Ferrario VF, Sforza C, Pizzini G, et al. (1993) Sexual dimorphism in the human face assessed by euclidean distance matrix analysis. J Anat 183, 593-600.
39. Ferrario VF, Sforza C, Poggio CE, et al. (1994) Distance from symmetry: a three-dimensional evaluation of facial asymmetry. J Oral Maxillofac Surg 52, 1126-1132.
40. Ferrario VF, Sforza C, Miani A, et al. (1995) A three-dimensional evaluation of human facial asymmetry. J Anat 186, 103-110.
41. Flury B (1987) Two generalizations of the common principal component model. Biometrika 74, 59-69.
42. Flury B (1988a) An application of common principal component analysis to cranial morphometry of Microtus californicus and M. ochrogaster (Mammalia, Rodentia). J Zool 216, 21-36.
43. Flury B (1988b) Common Principal Components and Related Multivariate Models. New York: Wiley.
44. Gangestad SW, Thornhill R (2003) Facial masculinity and fluctuating asymmetry. Evol Hum Behav 24, 231-241.
45. Gonzalez PN, Hallgrímsson B, Oyhenart E (2011) Developmental plasticity in covariance structure of the skull: effects of prenatal stress. J Anat 218, 243-257.
46. Goodall C (1991) Procrustes methods in the statistical analysis of shape. J R Stat Soc Series B (Methodol) 53, 285-339.
47. Graham JH, Raz S, Hel-Or H, et al. (2010) Fluctuating asymmetry: methods, theory and applications. Symmetry 2, 466-540.
48. Hamada H, Meno C, Watanabe D, et al. (2002) Establishment of vertebrate left-right asymmetry. Nat Rev Genet 3, 103-113.
49. Hamm J, Lee DD (2008) Grassman discriminant analysis: a unifying view on subspace-based learning. Proceedings of the 25th International conference on Machine Learning, pp. 376-383. Helsinki: ACM.
50. Hammer Ø, Harper D (2006) Paleontological Data Analysis. Oxford: Blackwell Publishing Ltd.
51. Hammond P, Hutton TJ, Allanson JE, et al. (2004) 3D analysis of facial morphology. Am J Hum Genet 126A, 339-348.
52. Hammond P, Forster-Gibson C, Chudley AE, et al. (2008) Face-brain asymmetry in autism spectrum disorders. Mol Psychiatry 13, 614-623.
53. Hennessy RJ, Kinsella A, Waddington JL (2002) 3D laser surface scanning and geometric morphometric analysis of craniofacial shape as an index of cerebro-craniofacial morphogenesis: initial application to sexual dimorphism. Biol Psychiatry 51, 507-514.
54. Hennessy RJ, Lane A, Kinsella A, et al. (2004) 3D morphometrics of craniofacial dysmorphology reveals sex-specific asymmetries in schizophrenia. Schizophr Res 67, 261-268.
55. Hennessy RJ, McLearie S, Kinsella A, et al. (2005) Facial surface analysis by 3D laser scanning and geometric morphometrics in relation to sexual dimorphism in cerebral-craniofacial morphogenesis and cognitive function. J Anat 207, 283-295.
56. Herler J, Kerschbaumer M, Mitteroecker P, et al. (2010) Sexual dimorphism and population divergence in the Lake Tanganyika cichlid fish genus Tropheus. Front Zool 7, 1-10.
57. Hill H, Claes P, Crocoran M, et al. (2011) How different is different? Criterion and sensitivity in face-space Front Psychol 2, 1-14.
58. Hutteger SM, Mitteroecker P (2011) Invariance and meaningfulness in phenotype space. Evol Biol 38, 335-351.
59. Hutton TJ, Buxton BF, Hammond P, et al. (2003) Estimating average growth trajectories in shape-space using kernel smoothing. IEEE Trans Med Imaging 22, 747-753.
60. Jones D (1995) Sexual selection, physical attractiveness, and facial neoteny. Curr Anthropo 36, 723-748.
61. Kimmerle EH, Jantz RL (2005) Secular trends in craniofacial asymmetry studied by geometric morphometry and generalized procrustes methods. In Modern Morphometrics in Physical Anthropology (ed Slice D), pp. 247-263. New York: Kluwer Academic/Plenum Publishers.
62. Kimmerle EH, Ross A, Slice D (2008) Sexual dimorphism in America: geometric morphometric analysis of the craniofacial region. J Forensic Sci 53, 54-57.
63. Kirkwood T (2010) Why women live longer. Sci Am 303, 34-35.
64. Klingenberg CP, McIntyre GS (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52, 1363-1375.
65. Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56, 1909-1920.
66. Klingenberg CP, Wetherill L, Rogers J, et al. (2010) Prenatal alcohol exposure alters the patterns of facial asymmetry. Alcohol 44, 649-657.
67. Knyazev AV, Argentati ME (2002) Principal angles between subspaces in an A-based scalar product: algorithms and perturbation estimates. SIAM J Sci Comput 23, 2008-2040.
68. Koehler N, Simmons WL, Rhodes G, et al. (2004) The relationship between sexual dimorphism in human faces and fluctuating asymmetry. Proc R Soc Lond B 271, 233-236.
69. Kranklin SB, Gibson DJ, Robertson PA, et al. (1995) Parallel analysis: a method for determining significant principal components. J Veg Sci 6, 99-106.
70. Krzanowski WJ (1979) Between-groups comparison of principal components. J Am Stat Assoc 74, 703-707.
71. Krzanowski WJ (1993) Permutational tests for correlation matrices. Stat Comput 3, 37-44.
72. Laurie CC (1997) The weaker sex is heterogametic: 75years of Haldane's rule. Genetics 147, 937-951.
73. Little AC, Jones BC, Waitt C, et al. (2008) Symmetry is related to sexual dimorphism in faces: data across culture and species. PLoS One 3, e2106.
74. Manly BFJ, Rayner JCW (1987) The comparison of sample covariance matrices using likelihood ratio tests. Biometrika 74, 841-847.
75. Mardia KV, Bookstein FL, Moreton IJ (2000) Statistical assessment of bilateral symmetry of shapes. Biometrika 87, 285-300.
76. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290-297.
77. Mitteroecker P, Bookstein FL (2009) The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution 63, 727-737.
78. Mitteroecker P, Bookstein FL (2011) Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 38, 100-114.
79. Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. J Evol Biol 36, 235-247.
80. Montagu A (1989) Growing Young. Westport, CT: Bergin & Garvey.
81. Obwegeser HL, Makek MS (1986) Hemimandibular hyperplasia - hemimandibular elongation. J Maxillofac Surg 14, 183-208.
82. Palmer AR (1994) Fluctuating asymmetry: a primer. In Developmental Instability: Its Origins and Implications (ed Markov T), pp. 335-364. Dordrecht: Kluwer.
83. Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17, 391-421.
84. Parsons KJ, Cooper WJ, Albertson RC (2009) Limits of principal component analysis for producing a common trait space: implications for inferring selection, contingency and chance in evolution. PLoS One 4, e7957.
85. Penton-Voak IS, Jones BC, Little AC, et al. (2001) Symmetry, sexual dimorphism in facial proportions and male face attractiveness. Proc R Soc Lond B 268, 1617-1623.
86. Pesarin F, Salmaso L (2010) Permutation Tests for Complex Data. West Sussex: John Wiley and Sons, Ltd.
87. Phillips PC, Arnold SJ (1999) Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution 53, 1506-1515.
88. Pretorius E, Steyn M, Scholtz Y (2006) Investigation into the usability of geometric morphometric analysis in assessment of sexual dimorphism. Am J Phys Anthropol 129, 64-70.
89. Puts DA (2010) Beauty and the beast: mechanisms of sexual selection in humans. Evol Hum Behav 31, 157-175.
90. Rohlf F, Slice D (1990) Extensions of the procrustus method for the optimal superimposition of landmarks. Syst Zool 39, 40-59.
91. Samal A, Subramani V, Marx D (2007) An analysis of sexual dimorphism in the human face. J Vis Commun Image Represent 18, 453-463.
92. Schaefer K, Fink B, Grammar K, et al. (2006a) Female appearance: facial and bodily attractiveness as shape. Psychol Sci 2, 187-204.
93. Schaefer K, Lauc T, Mitteroecker P, et al. (2006b) Dental arch asymmetry in an isolated Adriatic community. Am J Phys Anthropol 129, 132-142.
94. Scholtz Y, Pretorius E (2010) A geometric morphometric study inot the sexual dimorphism of the human scapula. J Comp Hum Biol 61, 253-270.
95. Scott IML, Pound N, Stephen ID, et al. (2010) Does masculinity matter? The contribution of masculine face shape to male attractiveness in humans PLoS One 5, e13585.
96. Shipley B (2000) A permutation procedure for testing the equality of pattern hypotheses across groups involving correlation or covariance matrices. Stat Comput 10, 253-257.
97. Smeets D, Claes P, Vandermeulen D, et al. (2010) Objective 3D face recognition: evolution, approaches and challenges. Forensic Sci Int 201, 125-132.
98. Smeets D, Claes P, Hermans J, et al. (2011a) A comparative study of 3D face recognition under expression variations. IEEE Trans Syst Man Cybern Part C Appl Rev, doi: 10.1109/TSMCC.2011.2174221.
99. Smeets D, Keustermans J, Hermans J, et al. (2011b) Symmetric surface-feature based 3D face recognition for partial data. The International Joint Conference on Biometrics, pp. 1-6. Washington, DC: IEEE Xplore.
100. Steppan SJ, Phillips PC, Houle D (2002) Comparative quantitative genetics: evolution of the G matrix. Trends Ecol Evol 17, 320-327.
101. Thomas CDL (2005) Three-dimensional quantification of facial shape. In: Computer-Graphic Facial Reconstruction (eds Clement JG, Marks MK), pp. 55-78. London: Elsevier Academic Press.
102. Uytterschaut HT (1986) Sexual dimorphism in human skulls. A comparison of sexual dimorphism in different populations. Hum Evol 1, 243-250.
103. Van Dongen S, Gangestad SW (2011) Human fluctuating asymmetry in relationship to health and quality: a meta-analysis. Evol Hum Behav 32, 380-398.
104. Van Valen L (1962) Study of fluctuating asymmetry. Evolution, 16, 125-142.
105. Viscosi V, Cardini A (2011) Leaf morphology, taxonomy and geometric morphometrics: a simplified protocol for beginners. PLoS One 6, e25630.
106. Walters M, Claes P, Kakulas E, et al. (in press a) 3D facial asymmetry assessment in hemimandibular hyperplasia and hemimandibular elongation anomalies. Int J Oral Maxillofac Surg, in press.
107. Wilkinson C (2010) Facial reconstruction - anatomical art or artistic anatomy? J Anat 216, 235-250.
108. Zaidel DW, Cohen JA (2005) The face, beauty, and symmetry: perceiving asymmetry in beautiful faces. Int J Neurosci 115, 1165-1173.