Epigenetic integration of the developing brain and face

Developmental Dynamics

Volumn 240, Issue 10, 2011, Pages 2233-2244

  Parsons, Trish E ^a,e   Schmidt, Eric J ^a   Boughner, Julia C ^b   Jamniczky, Heather A ^a   Marcucio, Ralph S ^c   Hallgrímsson, Benedikt ^a,d  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

^e UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Cleft lip; Computed microtomography; Face development; Geometric morphometrics; Integration; Mice; Modularity

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CORRELATION ANALYSIS; EMBRYO; EPIGENETICS; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; FACE DEVELOPMENT; FACE PROFILE; FOREBRAIN; MAMMAL; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGNATHIA; VERTEBRATE;

ANIMALS; BIOLOGICAL EVOLUTION; EPIGENESIS, GENETIC; FACE; HUMANS; MICE; MICE, INBRED STRAINS; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; PROSENCEPHALON;

MAMMALIA; MUS; VERTEBRATA;

EID: 80052969363     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22729     Document Type: Article

References (62)

1. Bastir M, Rosas A, Stringer C, Cuetara JM, Kruszynski R, Weber GW, Ross CF, Ravosa MJ. 2010. Effects of brain and facial size on basicranial form in human and primate evolution. J Hum Evol 58: 424-431.
2. Bergsma DR, Brown KS. 1975. Assessment of ophthalmologic, endocrinologic and genetic findings in the Bardet-Biedl syndrome. Birth Defects Orig Artic Ser 11: 132-136.
3. Biegert J. 1963. The evaluation of characteristics of the skull, hands and feet for primate taxonomy. In: Washburn SL, editor. Classification and human evolution. Chicago: Aldine. p 116-145.
4. Bookstein F. 2003. Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. J Human Evol 44: 167-187.
5. Bookstein FL. 1991. Morphometric tools for landmark data. Cambridge: Cambridge University Press.
6. Boughner JC, Hallgrímsson B. 2008. Biological spacetime and the temporal integration of functional modules: a case study of dento-gnathic developmental timing. Dev Dyn 237: 1-17.
7. Boughner JC, Wat S, Diewert VM, Young NM, Browder LW, Hallgrímsson B. 2008. Short-faced mice and developmental interactions between the brain and the face. J Anat 213: 646-662.
8. Breuker CJ, Patterson JS, Klingenberg CP. 2006. A single basis for developmental buffering of Drosophila wing shape. PLoS ONE 1: e7.
9. Cheverud JM. 1982. Phenotypic, genetic, and environmental integration in the cranium. Evolution 36: 499-516.
10. Cheverud JM. 1996. Developmental integration and the evolution of pleiotropy. Am Zool 36: 44-50.
11. Ciriani D, Diewert VM. 1986. A comparative study of development during primary palate formation in A/WySn, C57BL/6, and their F1 crosses. J Craniofac Genet Dev Biol 6: 369-377.
12. Creuzet S, Couly G, Le Douarin NM. 2005. Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J Anat 207: 447-459.
13. De Beer G. 1937. The development of the vertebrate skull. Oxford: Clarendon Press. xxiii, 552 p.
14. Diewert VM, Lozanoff S. 1993. Growth and morphogenesis of the human embryonic midface during primary palate formation analyzed in frontal sections. J Craniofac Genet Dev Biol 13: 162-183.
15. Diewert VM, Wang K-Y, Tait B. 1993. A new threshold model for cleft lip in mice. Ann NY Acad Sci 678: 341-343.
16. Enlow DH, McNamara JA. 1973. The neurocranial basis for facial form and pattern. Angle Orthodont 43: 256-270.
17. Goodall C. 1991. Procrustes methods in the statistical analysis of shape. J R Stat Soc B 53: 285-339.
18. Goswami A. 2006. Morphological integration in the carnivoran skull. Evol Int J Org Evolution 60: 169-183.
19. Hallgrímsson B, Lieberman DE. 2008. Mouse models and the evolutionary developmental biology of the skull. Integr Comp Biol 48: 373-384.
20. Hallgrímsson B, Brown JJ, Ford-Hutchinson AF, Sheets HD, Zelditch ML, Jirik FR. 2006. The brachymorph mouse and the developmental-genetic basis for canalization and morphological integration. Evol Dev 8: 61-73.
21. Hallgrímsson B, Lieberman DE, Liu W, Ford-Hutchinson AF, Jirik FR. 2007a. Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol Dev 9: 76-91.
22. Hallgrímsson B, Lieberman DE, Young NM, Parsons T, Wat S. 2007b. Evolution of covariance in the mammalian skull. Novartis Found Symp 284: 164-185; discussion 185-190.
23. Hallgrímsson B, Jamniczky H, Young N, Rolian C, Parsons T, Boughner J, Marcucio R. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36: 355-376.
24. Hansen TF, Houle D. 2008. Measuring and comparing evolvability and constraint in multivariate characters. J Evol Biol 21: 1201-1219.
25. Hendrikse JL, Parsons TE, Hallgrímsson B. 2007. Evolvability as the proper focus of evolutionary developmental biology. Evol Dev 9: 393-401.
26. Hu D, Marcucio RS. 2009a. A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 136: 107-116.
27. Hu D, Marcucio RS. 2009b. Unique organization of the frontonasal ectodermal zone in birds and mammals. Dev Biol 325: 200-210.
28. Hu D, Marcucio RS, Helms JA. 2003. A zone of frontonasal ectoderm regulates patterning and growth in the face. Development 130: 1749-1758.
29. Jamniczky HA, Boughner JC, Rolian C, Gonzalez PN, Powell CD, Schmidt EJ, Parsons TE, Bookstein FL, Hallgrimsson B. 2010. Rediscovering Waddington in the post-genomic age: operationalising Waddington's epigenetics reveals new ways to investigate the generation and modulation of phenotypic variation. Bioessays 32: 553-558.
30. Juriloff DM, Harris MJ, McMahon AP, Carroll TJ, Lidral AC. 2006. Wnt9b is the mutated gene involved in multifactorial nonsyndromic cleft lip with or without cleft palate in A/WySn mice, as confirmed by a genetic complementation test. Birth Defects Res A Clin Mol Teratol 76: 574-579.
31. Kile BT, Hentges KE, Clark AT, Nakamura H, Salinger AP, Liu B, Box N, Stockton DW, Johnson RL, Behringer RR, Bradley A, Justice MJ. 2003. Functional genetic analysis of mouse chromosome 11. Nature 425: 81-86.
32. Klingenberg CP. 2003. Developmental instability as a research tool: Using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. In: Polak M, editor. Developmental instability: causes and consequences. Oxford: Oxford University Press. p 427-442.
33. Klingenberg CP. 2005. Developmental constraints, modules and evolvability. In: Hallgrímsson B, Hall B, editors. Variation. Amsterdam: Elsevier Academic Press. p 219-248.
34. Klingenberg CP. 2008. Morphological integration and developmental modularity. Annu Rev Ecol Syst 39: 115-132.
35. Klingenberg CP. 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol Dev 11: 405-421.
36. Klingenberg CP. 2010. Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 11: 623-635.
37. Klingenberg CP. 2011. MORPHOJ: an integrated software package for geometric morphometrics. Mol Ecol Resources
38. Lieberman D. 2010. The evolution of the human head. Cambridge: Belknap Press of Harvard University Press.
39. Lieberman DE, Ross CF, Ravosa MJ. 2000. The primate cranial base: ontogeny, function, and integration. Am J Phys Anthropol(Suppl): 117-169.
40. Lieberman DE, Hallgrímsson B, Liu W, Parsons TE, Jamniczky HA. 2008. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J Anat 212: 720-735.
41. Marcucio RS, Cordero DR, Hu D, Helms JA. 2005. Molecular interactions coordinating the development of the forebrain and face. Dev Biol 284: 48-61.
42. Marroig G, Cheverud JM. 2001. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys. Evolution 55: 2576-2600.
43. Mitteroecker P. 2009. The developmental basis of variational modularity: Insights from quantitative genetics, morphometrics, and developmental biology. Evol Biol 36: 377-385.
44. Mitteroecker P, Bookstein F. 2008. The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution.
45. Parsons TE, Kristensen E, Hornung L, Diewert VM, Boyd SK, German RZ, Hallgrímsson B. 2008. Phenotypic variability and craniofacial dysmorphology: increased shape variance in a mouse model for cleft lip. J Anat 212: 135-143.
46. Rohlf FJ, Corti M. 2000. Use of two-block partial least-squares to study covariation in shape. Systemat Biol 49: 740-753.
47. Ross C, Henneberg M. 1995. Basicranial flexion, relative brain size, and facial kyphosis in Homo sapiens and some fossil hominids. Am J Phys Anthropol 98: 575-593.
48. Ross CF, Ravosa MJ. 1993. Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. Am J Phys Anthropol 91: 305-324.
49. Schmidt EJ, Parsons TE, Jamniczky HA, Gitelman J, Trpkov C, Boughner JC, Logan CC, Sensen CW, Hallgrímsson B. 2010. Micro-computed tomography-based phenotypic approaches in embryology: procedural artifacts in assessments of embryonic craniofacial growth and development. BMC Dev Biol 10: 18.
50. Sheets HD. 2004. IMP ThreeDStand6. http://www3.canisius.edu/~sheets/moremorph.html.
51. Spaventi R, Antica M, Pavelic K. 1990. Insulin and insulin-like growth factor I (IGF I) in early mouse embryogenesis. Development 108: 491-495.
52. Sulik KK, Johnston MC. 1982. Embryonic origin of holoprosencephaly: interrelationship of the developing brain and face. Scan Electron Microsc 309-322.
53. Szabo-Rogers HL, Smithers LE, Yakob W, Liu KJ. 2010. New Directions in craniofacial morphogenesis. Developmental Biology 341: 84-94.
54. Valeri CJ, Cole IIITM, Lele S, Richtsmeier JT. 1998. Capturing data from three-dimensional surfaces using fuzzy landmarks. Am J Phys Anthropol 107: 113-124.
55. Vermeij-Keers C, Mazzola RF, Van der Meulen JC, Strickler M. 1983. Cerebro-craniofacial and craniofacial malformations: an embryological analysis. Cleft Palate J 20: 128-145.
56. Waddington CH. 1942. The canalisation of development and the inheritance of acquired characters. Nature 150: 563.
57. Wagner GP, Altenberg L. 1996. Complex adaptations and the evolution of evolvability. Evolution 50: 967-976.
58. Wagner GP, Pavlicev M, Cheverud J. 2007. The road to modularity. Nat Genet 8: 921-931.
59. Wang KY, Juriloff DM, Diewert VM. 1995. Deficient and delayed primary palatal fusion and mesenchymal bridge formation in cleft lip-liable strains of mice. J Craniofac Genet Dev Biol 15: 99-116.
60. Weinberg SM, Andreasen NC, Nopoulos P. 2009. Three-dimensional morphometric analysis of brain shape in nonsyndromic orofacial clefting. J Anat 214: 926-936.
61. Young NM, Wat S, Diewert VM, Browder LW, Hallgrímsson B. 2007. Comparative morphometrics of embryonic facial morphogenesis: implications for cleft-lip etiology. Anat Rec (Hoboken) 290: 123-139.
62. Zelditch ML. 2004. Geometric morphometrics for biologists: a primer. Boston, MA: Elsevier Academic Press.