Evo-Devo insights from pathological networks: Exploring craniosynostosis as a developmental mechanism for modularity and complexity in the human skull

Journal of Anthropological Sciences

Volumn 93, Issue , 2015, Pages 103-117

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

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Craniosynostosis; Evolution; Human skull; Modularity; Morphological complexity; Networks

Indexed keywords

ADULT; ANATOMY AND HISTOLOGY; CRANIOFACIAL SYNOSTOSIS; EVOLUTION; GROWTH, DEVELOPMENT AND AGING; HUMAN; NEWBORN; PATHOLOGY; PHYSICAL ANTHROPOLOGY; PHYSIOLOGY; SKULL;

ADULT; ANTHROPOLOGY, PHYSICAL; BIOLOGICAL EVOLUTION; CRANIOSYNOSTOSES; HUMANS; INFANT, NEWBORN; SKULL;

EID: 84930682218     PISSN: 18274765     EISSN: None     Source Type: Journal    
DOI: 10.4436/JASS.93001     Document Type: Article

References (73)

1. Ackermann R. & Cheverud J. 2004. Morphological integration in primate evolution. In M. Pigliucci & K. Preston (eds): Phenotypic Integration. Studying the Ecology and Evolution of Complex Phenotypes, pp. 302-319. Oxford University Press, New York.
2. Bastir M. 2008. A systems-model for the morphological analysis of integration and modularity in human craniofacial evolution. J. Anthropol. Sci., 86: 37-58.
3. Bastir M. & Rosas A. 2013. Cranial airways and the integration between the inner and outer facial skeleton in humans. Am. J. Phys. Anthropol., 152: 287-293.
4. Callebaut W. & Rasskin-Gutman D. 2005. Modularity. Understanding the Development and Evolution of Natural Complex Systems. MIT Press, Cambridge.
5. Cheverud J. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36: 499-516.
6. Cohen M.M. & MacLean R.E. 2000. Craniosynostosis. Diagnosis, Evaluation, and Management. Oxford University Press, New York.
7. Cohen M.M. 2000. Epidemiology of craniosynostosis. In M.M.Jr. Cohen & R.E. MacLean (eds): Craniosynostosis. Diagnosis, Evaluation, and Management, 2nd Edition, pp. 112-118. Oxford University Press, New York.
8. Corner B.D. & Richtsmeier J.T. 1992. Experiments of nature: premature unicoronal cranial synostosis in mantled howler monkeys (Alouatta palliata). Cleft Palate-Cran. J., 29: 143-151.
9. Couly G.F., Coltey P.M. & Douarin N.M.L. 1993. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development, 117: 409-429.
10. Cray J.Jr., Cooper G.M., Mooney M.P. & Siegel M.I. 2012. Ectocranial suture fusion in primates: as related to cranial volume and dental eruption. J. Med. Primatol., 41: 356-363.
11. Derderian C. & Seaward J. 2012. Syndromic craniosynostosis. Semin. Plas. Surg., 26: 64-75.
12. Di Ieva A., Bruner E., Davidson J., Pisano P., Haider T., Stone S.S., Cusimano M.D., Tschabitscher M. & Grizzi F. 2013. Cranial sutures: a multidisciplinary review. Childs Nerv. Syst., 29:893-905.
13. Eble G.J. 2005. Morphological modularity and macroevolution: conceptual and empirical aspects. In W. Callebaut & D. Rasskin-Gutman (eds): Modularity. Understanding the Development and Evolution of Natural Complex Systems, pp. 221-238. MIT Press, Cambridge.
14. Esteve-Altava B. 2013. Structural Analysis of Network Models in Tetrapod Skulls: Evolutionary Trends and Structural Constraints in Morphological Complexity, Integration and Modularity (Ph.D. Thesis). University of Valencia, Spain. Retrieved from http://roderic.uv.es/handle/10550/31487.
15. Esteve-Altava B. & Rasskin-Gutman D. 2014. Theoretical morphology of tetrapod skull networks. C. R. Palevol, 13: 41-50.
16. Esteve-Altava B., Marugán-Lobón J., Botella H. & Rasskin-Gutman D. 2011. Network models in anatomical systems. J. Anthropol. Sci., 89: 175-184.
17. Esteve-Altava B., Marugán-Lobón J., Botella H. & Rasskin-Gutman D. 2014. Random loss and selective fusion of bones originate morphological complexity trends in tetrapod skull networks. Evol. Biol., 41: 52-61.
18. Esteve-Altava B., Marugán-Lobón J., Botella H., Bastir M. & Rasskin-Gutman D. 2013a. Grist for Riedl’s mill: a network model perspective on the integration and modularity of the human skull. J. Exp. Zool. (Mol. Dev. Evol.), 320: 489-500.
19. Esteve-Altava B., Marugán-Lobón J., Botella H. & Rasskin-Gutman D. 2013b. Structural constraints in the evolution of the tetrapod skull complexity: Williston’s law revisited using network models. Evol. Biol., 40: 209-219.
20. Esteve-Altava B., Marugán-Lobón J., Botella H. & Rasskin-Gutman D. 2014. Random loss and selective fusion of bones originate morphological complexity trends in tetrapod skull networks. Evol. Biol., 41: 52-61.
21. Falk D., Zollikofer, C.P.E., Morimoto, N. & Ponce de León, M.S. 2012. Metopic suture of Taung (Australopithecus africanus) and its implications for hominin brain evolution. Proc. Natl. Acad, Sci. U.S.A., 109: 8467-8470.
22. Garza R.M. & Khosla R.K. 2012. Nonsyndromic craniosynostosis. Semin. Plas. Surg., 26: 53-63.
23. 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.
24. Goodwin B.C, Kauffman, S. & Murray J.D. 1993. Is morphogenesis and intrinsically robust process? J. Theor. Biol., 163: 135-144.
25. Goswami A. 2007. Cranial modularity and sequence heterochrony in mammals. Evol. Dev., 9: 290-298.
26. Gracia A., Arsuaga J.L., Carretero J.M., Bermúdez de Castro, J.M. & Carbonell E. 2009. Craniosynostosis in the Middle Pleistocene human cranium 14 from Sima de los Huesos, Atapuerca, Spain. Proc. Natl. Acad, Sci. U.S.A., 106: 6573-6578.
27. Gracia A., Martínez-Lage J.F., Arsuaga J.L., Martínez I., Lorenzo C. & Pérez-Espejo, M.A. 2010. The earliest evidence of true lambdoid craniosynostosis: the case of “Benjamina”, a Homo heidelbergensis child. Child. Nerv. Syst., 26: 723-727.
28. Gray H. 1918. Anatomy of the Human Body. Lea and Febiger, Philadelphia.
29. Gregory W.K. 1934. Polyisomerism and anisomerism in cranial and dental evolution among vertebrates. Proc. Natl. Acad, Sci. U.S.A., 20: 1-9.
30. Gregory W.K. 1935. Williston’s law relating to the evolution of skull bones in the vertebrates. Am. J. Phys. Anthropol., 20: 123-152.
31. Hallgrimsson B. & Lieberman D.E. 2008. Mouse models and the evolutionary developmental biology of the skull. Integr. Comp. Biol., 48: 373-384.
32. Heuzé Y., Boyadjiev S.A., Marsh J.L., Kane A.A., Cherkez E., Boggan J.E. & Richtsmeier J.T. 2010. New insights into the relationship between suture closure and craniofacial dysmorphology in sagittal nonsyndromic craniosynostosis. J. Anat., 217: 85-96.
33. Holton N.E., Yokley T.R., Froehle A.W. & Southard T.E. 2014. Ontogenetic scaling of the human nose in a longitudinal sample: Implications for genus Homo facial evolution. Am. J. Phys. Anthropol., 153: 42-60.
34. Heuzé Y., Martínez-Abadías N., Stella J.M., Senders C.W., Boyadjiev S.A., Lo L.J. & Richtsmeier J.T. 2012. Unilateral and bilateral expression of a quantitative trait: asymmetry and symmetry in coronal craniosynostosis. J. Exp. Zool. (Mol. Dev. Evol.), 318: 109-122.
35. Hukki J, Saarinen P, Kangasniemi M. 2008. Single suture craniosynostosis: diagnosis and imaging. In D.P. Rice (ed): Craniofacial Sutures Development, Disease, and Treatment, pp. 79-90. Karger, Basel.
36. Klingenberg C.P. 2008. Morphological integration and developmental modularity. Ann. Rev. Ecol. Evol. S., 39: 115-132.
37. Koyabu D., Maier W. & Sánchez-Villagra M.R. 2012. Paleontological and developmental evidence resolve the homology and dual embryonic origin of a mammalian skull bone, the interparietal. Proc. Natl. Acad, Sci. U.S.A., 109: 14075-14080.
38. Krogman W.M. 1930. Studies in growth changes in the skull and face of anthropoids: ectocranial and endocranial suture closure in anthropoids and Old World apes. Am. J. Phys. Anthropol., 46: 315-353.
39. Laue K., Pogoda H.M., Daniel P.B., van Haeringen A., Alanay Y., von Ameln S., Rachwalski M., Morgan T., Gray M.J., Breuning M.H., Sawyer G.M., Sutherland-Smith A.J., Nikkels P.G., Kubisch C., Bloch W., Wollnik B., Hammerschmidt M. & Robertson S.P. 2011. Craniosynostosis and multiple skeletal anomalies in humans and zebrafish result from a defect in the localized degradation of retinoic acid. Am. J. Hum. Genet., 89: 595-606.
40. Lieberman D.E. 2011. The evolution of the human head. Harvard University Press, Cambridge.
41. Marchac D., Renier D. & Arnaud E. 2008. Unoperated craniosynostosis patients: correction in adulthood. Plast. Reconstr. Surg., 122: 1827-1838.
42. Martínez-Abadías N., Esparza M., Sjovold T., González-Jose R., Santos M., Hernandez M. 2009. Heritability of human cranial dimensions: comparing the evolvability of different cranial regions. J. Anat., 214: 19-35.
43. Martínez-Abadías N., Percival C., Aldridge K., Hill C.A., Ryan T., Sirivunnabood S., Wang Y., Jabs E.W. & Richtsmeier J.T. 2010. Beyond the closed suture in Apert syndrome mouse models: evidence of primary effects of FGFR2 signaling on facial shape at birth. Dev. Dynam., 239: 3058-3071.
44. Martínez-Abadías N., Heuzé Y., Wang Y., Jabs E.W., Aldridge K. & Richtsmeier J.T. 2011. FGF/FGFR signaling coordinates skull development by modulating magnitude of morphological integration: evidence from Apert syndrome mouse models. PLoS ONE, 6: e26425.
45. Martínez-Abadías N., Mitteroecker P., Parsons T.E., Esparza M., Sjøvold T., Rolian C., Richtsmeier J.T. & Hallgrimsson B. 2012. The developmental basis of quantitative craniofacial variation in humans and mice. Evol. Biol., 39: 554-567.
46. McShea D.W. & Brandon R.N. 2010. Biology’s First Law. University of Chicago Press, Chicago.
47. McShea D.W. & Hordijk W. 2013. Complexity by subtraction. Evol. Biol., 40: 504-520.
48. McShea D.W. 1991. Complexity and evolution: what everybody knows. Biol. Philos., 6: 303-324.
49. McShea, D.W. 1993. Evolutionary change in the morphological complexity of the mammalian vertebral column. Evolution, 47: 730-740.
50. Mitteroecker P. & Bookstein, F.L. 2008. The evolutionary role of modularity and integration in the hominoid cranium. Evolution, 62: 943-958.
51. Mitteroecker P., Gunz P., Neubauer S. & Müller, G. 2012. How to explore morphological integration in human evolution and development? Evol. Biol., 39: 536-553.
52. Morriss-Kay G.M. 2001. Derivation of the mammalian skull vault. J. Anat., 199: 143-151.
53. Moss M.L. & Young R.W. 1960. A functional approach to craniology. Am. J. Phys. Anthropol., 48: 1747-1763.
54. Motch Perrine S.M., Cole T.M., Martínez-Abadías N, Aldridge K., Jabs E.W. & Richtsmeier J.T. 2014. Craniofacial divergence by distinct prenatal growth patterns in Fgfr2 mutant mice. BMC Dev. Biol., 14:8.
55. Olson E.C. & Miller R.L. 1958. Morphological Integration. University of Chicago Press, Chicago.
56. Rice D.P. 2008. Craniofacial Sutures Development, Disease and Treatment. Karger, Basel.
57. Rasskin-Gutman D. & Esteve-Altava B. 2014. Connecting the dots: Anatomical network analysis in morphological EvoDevo. Biol. Theory, 9: 178-193.
58. Richtsmeier J.T. & DeLeon V.B. 2009. Morphological integration of the skull in craniofacial anomalies. Orthod. Craniofac. Res., 12: 149-158.
59. Richtsmeier J.T., Aldridge K., DeLeon V.B., Panchal J., Kane A.A., Marsh J.L., Yan P., Cole T.M. III. 2006. Phenotypic integration of neurocranium and brain. J. Exp. Zool. (Mol. Dev. Evol.), 306: 360-378.
60. Sánchez-Lara P.A., Graham J.M.Jr., Hing A.V., Lee J. & Cunningham M. 2007. The morphogenesis of wormian bones: a study of craniosynostosis and purposeful cranial deformation. Am. J. Med. Genet. Part A, 143: 3243-3251.
61. Santagati F. & Rijli F.M. 2003. Cranial neural crest and the building of the vertebrate head. Nat. Rev. Neurosci., 4: 806-818.
62. Schlosser G. & Wagner GP. 2004. Modularity in Development and Evolution. University of Chicago Press, Chicago.
63. Schoch R.R. 2006. Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades. Evol. Dev., 8: 524-536.
64. Shea B.T. 1989. Heterochrony in human evolution: the case for neoteny reconsidered. Yearb. Phys. Anthropol., 32: 69-101.
65. Sidor C.A. 2001. Simplification as a trend in synapsid cranial evolution. Evolution, 55: 1419-1442.
66. Simon HA. 1962. The architecture of complexity. P. Am. Philos. Soc., 106: 467-482
67. Singh N., Harvati K., Hublin J.J. & Klingenberg C.P. 2012. Morphological evolution through integration: a quantitative study of cranial integration in Homo, Pan, Gorilla and Pongo. J. Hum. Evol., 62: 155-164.
68. Williston S.W. 1914. Water reptiles of the past and present. University of Chicago Press, Chicago.
69. Wilson L.A.B. & Sánchez-Villagra M.R. 2009. Heterochrony and patterns of cranial suture closure in hystricognath rodents. J. Anat., 214: 339-335.
70. Wilson L.A.B. 2013. Cranial suture closure patterns in sciuridae: heterochrony and modularity. J. Mammal Evol., doi: 10.1007/s10914-013-9242-5.
71. Wu J.K., Goodrich J.T., Amadi C.C., Miller T., Mulliken J.B. & Shanske A.L. 2011. Interparietal bone (Os Incae) in craniosynostosis. Am. J. Med. Genet. A, 155: 287-294.
72. Zollikofer C.P.E. & Ponce de León M.S. 2008. Cranial growth models: heterochrony, heterotopy, and the kinematics of ontogeny. In K. Harvati & T. Harrison (eds): Neanderthals Revisited: New Approaches and Perspectives, pp. 89-112. Springer, New York.
73. Zollikofer C.P.E. & Ponce de León M.S. 2010. The evolution of hominin ontogenies. Semin. Cell Dev. Biol., 21: 441-452.