Beyond the functional matrix hypothesis: A network null model of human skull growth for the formation of bone articulations

Journal of Anatomy

Volumn 225, Issue 3, 2014, Pages 306-316

  Esteve Altava, Borja ^a   Rasskin Gutman, Diego ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Anatomical networks; Epigenetics; Gabriel rule; Head development; Morphology

Indexed keywords

ALGORITHM; ANATOMY AND HISTOLOGY; BIOLOGICAL MODEL; BONE DEVELOPMENT; BONE MATRIX; CRANIAL SUTURE; EVOLUTION; FACIAL BONE; GROWTH, DEVELOPMENT AND AGING; HUMAN; SKULL;

ALGORITHMS; BIOLOGICAL EVOLUTION; BONE DEVELOPMENT; BONE MATRIX; CRANIAL SUTURES; FACIAL BONES; HUMANS; MODELS, BIOLOGICAL; SKULL;

EID: 84905568011     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12212     Document Type: Article

References (83)

1. Aldridge K, Kane AA, Marsh JL, et al. (2005) Brain morphology in nonsyndromic unicoronal craniosynostosis. Anat Rec 285, 690-698.
2. Bastir M, Rosas A, O'Higgins P (2006) Craniofacial levels and the morphological maturation of the human skull. J Anat 209, 637-654.
3. Bastir M, Rosas A, Lieberman DE, et al. (2008) Middle cranial fossa anatomy and the origin of modern humans. Anat Rec 291, 130-140.
4. Bastir M, Rosas A, Stringer C, et al. (2010) Effects of brain and facial size on basicranial form in human and primate evolution. J Hum Evol 58, 424-431.
5. Bastir M, Rosas A, Gunz P, et al. (2011) Evolution of the base of the brain in highly encephalized human species. Nat Commun 2, 588.
6. Borg I, Groenen PJF (2005) Modern Multidimensional Scaling: Theory and Applications. New York: Springer.
7. Breitsprecher L, Fanghanel L, Noe A, et al. (2002) The functional anatomy of the muscles of facial expression in humans with and without cleft lip and palate. A contribution to refine muscle reconstruction in primary cheilo- and rhinoplasties in patients with uni- and bilateral complete CLP. Ann Anat 184, 27-34.
8. Bruner E (2004) Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J Hum Evol 47, 279-303.
9. Bruner E, De la Cuétara JM, Masters M, et al. (2014) Functional craniology and brain evolution: from paleontology to biomedicine. Front Neuroanat 8, 00019.
10. 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.
11. Cheverud JM (1982) Phenotypic, genetic, and enviromental morphological integration in the cranium. Evolution 36, 499-516.
12. Cohen MM Jr, MacLean RE (2000) Craniosynostosis: Diagnosis, Evaluation, and Management. Oxford: Oxford University Press.
13. Cray J Jr, Cooper GM, Mooney MP, et al. (2012) Ectocranial suture fusion in primates: as related to cranial volume and dental eruption. J Med Primatol 41, 356-363.
14. Curtis N, Witzel U, Fagan MJ (2014) Development and three-dimensional morphology of the zygomaticotemporal suture in primate skulls. Folia Primatol 85, 77-87.
15. Depew MJ, Simpson CA (2006) 21st century neontology and the comparative development of the vertebrate skull. Dev Dyn 235, 1256-1291.
16. Depew MJ, Compagnucci C, Griffin J (2008) Suture neontology and paleontology: The bases for where, when and how boundaries between bones have been established and have evolved. In: Craniofacial Sutures, Development, Disease and Treatment. (ed. Rice DP), pp. 57-78. London: Karger.
17. Di Ieva A, Bruner E, Davidson J, et al. (2013) Cranial sutures: a multidisciplinary review. Childs Nerv Syst 29, 893-905.
18. Dorogovtsev R, Mendes JFF (2003) Evolution of Networks: from Biological Networks to the Internet and WWW. Oxford: Oxford University Press.
19. Enlow DH, Hans MG (1996) Essentials of Facial Growth. Philadelphia: WB Saunders.
20. Esteve-Altava B, Rasskin-Gutman D (2014) Theoretical morphology of tetrapod skull networks. CR Palevol 13, 41-50.
21. Esteve-Altava B, Marugán-Lobón J, Botella H, et al. (2011) Network models in anatomical systems. J Anthropol Sci 89, 175-184.
22. Esteve-Altava B, Marugán-Lobón J, Botella H, et al. (2013a) Grist for Riedl's mill: a network model perspective on the integration and modularity of the human skull. J Exp Zool B Mol Dev Evol 320, 489-500.
23. Esteve-Altava B, Marugán-Lobón J, Botella H, et al. (2013b) Structural constraints in the evolution of the tetrapod skull complexity: Williston's law revisited using network models. Evol Biol 40, 209-219.
24. Esteve-Altava B, Marugán-Lobón J, Botella H, et al. (2014) Random loss and selective fusion of bones originate morphological complexity trends in tetrapod skull networks. Evol Biol 41, 52-61.
25. Falk D, Zollikofer CP, Morimoto N, et al. (2012) Metopic suture of Taung (Australopithecus africanus) and its implications for hominin brain evolution. Proc Natl Acad Sci USA 109, 8467-8470.
26. Festa F, Capasso L, D'Anastasio R, et al. (2010) Maxillary and mandibular base size in ancient skulls and of modern humans from Opi, Abruzzi, Italy: a cross-sectional study. World J Orthod 11, e1-e4.
27. Fields HWJ, Metzner L, Garol JD, et al. (1978) The craniofacial skeleton in anencephalic human fetuses. I. Cranial floor. Teratology 17, 57-65.
28. Gabriel KR, Sokal RR (1969) A new statistical approach to geographic variation analysis. Syst Zool 18, 259.
29. Hall BK (1994) Homology: The Hierarchical Basis of Comparative Biology. San Diego: Academic Press.
30. Hall JG (2010) Importance of muscle movement for normal craniofacial development. J Craniofac Surg 21, 1336-1338.
31. Herring SW (2008) Mechanical influences on suture development and patency. In: Craniofacial Sutures, Development, Disease and Treatment. (ed. Rice DP), pp. 41-56. London: Karger.
32. Hirabayashi S, Harii K, Sakurai A, et al. (1988) An experimental study of craniofacial growth in a heterotopic rat head transplant. Plast Reconstr Surg 82, 236-243.
33. Humphries MD, Gurney K (2008) Network 'small-world-ness': a quantitative method for determining canonical network equivalence. PLoS ONE 3, e0002051.
34. Karsenty G (1999) The genetic transformation of bone biology. Genes Dev 13, 3037-3051.
35. Khonsari RH, Olivier J, Vigneaux P, et al. (2013) A mathematical model for mechanotransduction at the early steps of suture formation. Proc Biol Sci 280, 20122670.
36. Kikuchi M (2005) Orthodontic treatment in children to prevent sleep-disordered breathing in adulthood. Sleep Breath 9, 146-158.
37. Koyabu D, Werneburg I, Morimoto N, et al. (2014) Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size. Nat Commun 5, 3625.
38. Kruskal JB, Wish M (1978) Multidimensional Scaling. Beverly Hills: Sage Publications.
39. Li A, Horvath S (2007) Network neighborhood analysis with the multi-node topological overlap measure. Bioinformatics 23, 222-231.
40. Lieberman DE (2011a) Epigenetic integration, complexity, and evolvability of the head: rethinking the functional matrix hypothesis. In: Epigenetics: Linking Genotype and Phenotype in Development and Evolution. (eds Hallgrimsson B, Hall BK), pp. 271-289, Los Angeles: California University Press.
41. Lieberman DE (2011b) The Evolution of the Human Head. London: Belknap Press.
42. Marazita ML, Mooney MP (2004) Current concepts in the embryology and genetics of cleft lip and cleft palate. Clin Plast Surg 31, 125-140.
43. McBratney-Owen B, Iseki S, Bamforth SD, et al. (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322, 121-132.
44. Morriss-Kay GM (2001) Derivation of the mammalian skull vault. J Anat 199, 143-151.
45. Moss ML (1968) A theoretical analysis of the functional matrix. Acta Biotheor 18, 195-202.
46. Moss ML (1975) New studies of cranial growth. Birth Defects Orig Artic Ser 11, 283-295.
47. Moss ML (2007) The differential roles of periosteal and capsular functional matrices in orofacial growth. Euro J Orthod 29, i96-i101.
48. Moss ML, Greenberg SN (1967) Functional cranial analysis of the human maxillary bone: I, Basal bone. Angle Orthod 37, 151-164.
49. Moss ML, Salentijn L (1969a) The capsular matrix. Am J Orthod 56, 474-490.
50. Moss ML, Salentijn L (1969b) The primary role of functional matrices in facial growth. Am J Orthod 55, 566-577.
51. Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18, 281-292.
52. Mulliken JB, Ferraro NF, Vento AR (1989) A retrospective analysis of growth of the constructed condyle-ramus in children with hemifacial microsomia. Cleft Palate J 26, 312-317.
53. Neubauer S, Gunz P, Hublin JJ (2009) The pattern of endocranial ontogenetic shape changes in humans. J Anat 215, 240-255.
54. Newman MEJ (2005) Power laws, Pareto distributions and Zipf's law. Contemp Phys 46, 323-351.
55. Newman ME, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E 69, 026113.
56. Nonaka K, Nakata M (1984) Genetic variation and craniofacial growth in inbred rats. J Craniofac Genet Dev Biol 4, 271-302.
57. Opperman LA (2000) Cranial sutures as intramembranous bone growth sites. Dev Dyn 219, 472-485.
58. Opperman LA, Passarelli RW, Nolen AA, et al. (1996) Dura mater secretes soluble heparin-binding factors required for cranial suture morphogenesis. In Vitro Cell Dev Biol 32, 627-632.
59. Pritchard JJ, Scott JH, Girgis FG (1956) The structure and development of cranial and facial sutures. J Anat 90, 73-86.
60. Quarto N, Longaker MT (2008) The zebrafish (Danio rerio): a model system for cranial suture patterning. Cells Tissues Organs 181, 109-118.
61. Rasskin-Gutman D (2003) Boundary constraints for the emergence of form. In: Origination of Organismal Form. (eds Müller G, Newman S), pp. 305-322, Cambridge: The MIT Press.
62. Rasskin-Gutman D, Esteve-Altava B (2014) Connecting the dots: anatomical network analysis in morphological EvoDevo. Biol Theory 9, 178-193.
63. Ravasz E, Barabási A-L (2003) Hierarchical organization in complex networks. Phys Rev E 67, 026112.
64. Ravasz E, Somera AL, Mongru DA, et al. (2002) Hierarchical organization of modularity in metabolic networks. Science 297, 1551-1555.
65. Rice DP (2008) Craniofacial Sutures: Development, Disease, and Treatment. Basel: Karger.
66. Richards GD, Jabbour RS (2011) Foramen magnum ontogeny in Homo sapiens: a functional matrix perspective. Anat Rec 294, 199-216.
67. Richtsmeier JT, Flaherty K (2013) Hand in glove: brain and skull in development and dysmorphogenesis. Acta Neuropathol 125, 469-489.
68. Richtsmeier JT, Aldridge K, DeLeon VB, et al. (2006) Phenotypic integration of neurocranium and brain. J Exp Zool B Mol Dev Evol 306, 360-378.
69. Sardi ML, Ramirez Rozzi F, Pucciarelli HM (2004) The neolithic transition in Europe and North Africa. The functional craneology contribution. Anthropol Anz 62, 129-145.
70. Shwartz Y, Farkas Z, Stern T, et al. (2012) Muscle contraction controls skeletal morphogenesis through regulation of chondrocyte convergent extension. Dev Biol 370, 154-163.
71. Singh N, Harvati K, Hublin JJ, et al. (2012) Morphological evolution through integration: a quantitative study of cranial integration in Homo, Pan, Gorilla and Pongo. J Hum Evol 62, 155-164.
72. Singleton M (2012) Postnatal cranial development in papionin primates: an alternative model for hominin evolutionary development. Evol Biol 39, 499-520.
73. Smith DW, Tondury G (1978) Origin of the calvaria and its sutures. Am J Dis Child 132, 662-666.
74. Smith TD, Rossie JB, Cooper GM, et al. (2010) The maxillary sinus in three genera of new world monkeys: factors that constrain secondary pneumatization. Anat Rec 293, 91-107.
75. Solé RV, Valverde S, Rodríguez-Caso C (2006) Modularity in biological networks. In: Biological Networks. (ed. Képès F), pp. 21-40. Singapore: World Scientific.
76. Sperber GH, Sperber MS, Guttmann GD (2010) Craniofacial Embriogenetics and Development. Shelton: People's Medical Publishing House-USA.
77. Sugawara Y, Hirabayashi S, Harii K (1999) Craniofacial growth in a whole rat head transplant: how does a non-functional head grow? J Craniofac Genet Dev Biol 19, 102-108.
78. Ten Cate AR, Freeman E, Dickinson JB (1977) Sutural development: structure and its response to rapid expansion. Am J Orthod 71, 622-636.
79. Watts DJ, Strogatz SH (1998) Collective dynamics of 'small-world' networks. Nature 393, 440-442.
80. Wuchty S, Ravasz E, Barabási A-L (2006) The architecture of biological networks. In:Complex Systems Science in Biomedicine. (eds Deisboeck TS, Kresh JT), pp. 165-181. New York, NY: Springer.
81. Yip AM, Horvath S (2007) Gene network interconnectedness and the generalized topological overlap measure. BMC Bioinformatics 8, 22.
82. Zhang G, Eames BF, Cohn MJ (2009) Evolution of vertebrate cartilage development. Curr Top Dev Biol 86, 15-42.
83. Zollikofer CP, Ponce de Leon MS (2010) The evolution of hominin ontogenies. Semin Cell Dev Biol 21, 441-452.