Genetics of murine craniofacial morphology: Diallel analysis of the eight founders of the Collaborative Cross

Journal of Anatomy

Volumn 228, Issue 1, 2016, Pages 96-112

  Percival, Christopher J ^a,b   Liberton, Denise K ^a,b,f   Pardo Manuel de Villena, Fernando ^c   Spritz, Richard ^d   Marcucio, Ralph ^e   Hallgrímsson, Benedikt ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

Collaborative cross; Craniofacial form; Diallel; Micro computed tomography; Morphometrics; Mouse models; Normal variation

Indexed keywords

ANATOMY AND HISTOLOGY; ANIMAL; CROSS BREEDING; FOUNDER EFFECT; GENETIC ASSOCIATION STUDY; GENETIC VARIATION; GENOTYPE; INBRED MOUSE STRAIN; MOUSE; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE TRAIT LOCUS; SKULL;

ANIMALS; CROSSES, GENETIC; FOUNDER EFFECT; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENOTYPE; MICE; MICE, INBRED STRAINS; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE TRAIT LOCI; SKULL;

EID: 84955171314     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12382     Document Type: Article

References (73)

1. Abzhanov A, Tabin CJ (2004) Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Dev Biol 273, 134-148.
2. Abzhanov A, Protas M, Grant BR, et al. (2004) Bmp4 and morphological variation of beaks in Darwin's finches. Science 305, 1462-1465.
3. Abzhanov A, Kuo WP, Hartmann C, et al. (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 442, 563-567.
4. Albertson RC, Streelman JT, Kocher TD (2003) Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc Natl Acad Sci U S A 100, 5252-5257.
5. Alexander C, Piloto S, Le Pabic P, et al. (2014) Wnt signaling interacts with Bmp and Edn1 to regulate dorsal-ventral patterning and growth of the craniofacial skeleton. PLoS Genet 10, e1004479.
6. Auffray J-C, Alibert P, Latieule C, et al. (1996) Relative warp analysis of skull shape across the hybrid zone of the house mouse (Mus musculus) in Denmark. J Zool 240, 441-455.
7. Beck JA, Lloyd S, Hafezparast M, et al. (2000) Genealogies of mouse inbred strains. Nat Genet 24, 23-25.
8. Boyko AR, Quignon P, Li L, et al. (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8, 1-13.
9. Brugmann SA, Goodnough LH, Gregorieff A, et al. (2007) Wnt signaling mediates regional specification in the vertebrate face. Development 134, 3283-3295.
10. Buchtová M, Kuo WP, Nimmagadda S, et al. (2010) Whole genome microarray analysis of chicken embryo facial prominences. Dev Dyn 239, 574-591.
11. Burgio G, Baylac M, Heyer E, et al. (2009) Genetic analysis of skull shape variation and morphological integration in the mouse using interspecific recombinant congenic strains between C57BL/6 and mice of the Mus spretus species. Evolution 63, 2668-2686.
12. Carlborg Ö, Haley CS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5, 618-625.
13. Chai Y, Maxson RE Jr (2006) Recent advances in craniofacial morphogenesis. Dev Dyn 235, 2353-2375.
14. Chesler EJ, Miller DR, Branstetter LR, et al. (2008) The Collaborative Cross at Oak Ridge National Laboratory: developing a powerful resource for systems genetics. Mamm Genome 19, 382-389.
15. Cheverud JM (1982) Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36, 499-516.
16. Cheverud JM (1996a) Developmental integration and the evolution of pleiotropy. Am Zool 36, 44-50.
17. Cheverud JM (1996b) Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. J Evol Biol 9, 5-42.
18. Cheverud JM, Routman EJ, Irschick DJ (1997) Pleiotropic effects of individual gene loci on mandibular morphology. Evolution 51, 2006-2016.
19. Chong HJ, Young NM, Hu D, et al. (2012) Signaling by SHH rescues facial defects following blockade in the brain. Dev Dyn 241, 247-256.
20. Churchill GA, Airey DC, Allayee H, et al. (2004) The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat Genet 36, 1133-1137.
21. Claes P, Liberton DK, Daniels K, et al. (2014) Modeling 3D facial shape from DNA. PLoS Genet 10, e1004224.
22. Collaborative Cross Consortium (2012) The genome architecture of the Collaborative Cross mouse genetic reference population. Genetics 190, 389-401.
23. Drake AG, Klingenberg CP (2008) The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B Biol Sci 275, 71-76.
24. Feng W, Leach SM, Tipney H, et al. (2009) Spatial and temporal analysis of gene expression during growth and fusion of the mouse facial prominences. PLoS ONE 4, e8066.
25. Gerasimov S, Nikolov H, Mihailova V, et al. (1990) Morphometric stepwise discriminant analysis of the five genetically determined European taxa of the genus Mus. Biol J Linn Soc 41, 47-64.
26. Griffin JN, Compagnucci C, Hu D, et al. (2013) Fgf8 dosage determines midfacial integration and polarity within the nasal and optic capsules. Dev Biol 374, 185-197.
27. Hallgrímsson B, Lieberman DE, Liu W, et al. (2007) Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol Dev 9, 76-91.
28. Hallgrímsson B, Jamniczky H, Young NM, et al. (2009) Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36, 355-376.
29. Hemani G, Knott S, Haley C (2013) An evolutionary perspective on epistasis and the missing heritability. PLoS Genet 9, e1003295.
30. Hill WG, Goddard ME, Visscher PM (2008) Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet 4, e1000008.
31. Hu D, Marcucio RS (2009) A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 136, 107-116.
32. Ingram DK, Reynolds MA, Les EP (1982) The relationship of genotype, sex, body weight, and growth parameters to lifespan in inbred and hybrid mice. Mech Ageing Dev 20, 253-266.
33. Johannsdottir B, Thorarinsson F, Thordarson A, et al. (2005) Heritability of craniofacial characteristics between parents and offspring estimated from lateral cephalograms. Am J Orthod Dentofac Orthop 127, 200-207.
34. Keane TM, Goodstadt L, Danecek P, et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477, 289-294.
35. Kimura T, Shimada A, Sakai N, et al. (2007) Genetic analysis of craniofacial traits in the medaka. Genetics 177, 2379-2388.
36. Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11, 353-357.
37. Klingenberg CP, Leamy LJ, Routman EJ, et al. (2001) Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics. Genetics 157, 785-802.
38. Klingenberg CP, Leamy LJ, Cheverud JM (2004) Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics 166, 1909-1921.
39. Kohn L (1991) The role of genetics in craniofacial morphology and growth. Annu Rev Anthropol 20, 261-278.
40. Kurnianto E, Shinjo A, Suga D, et al. (1999) Diallel cross analysis of body weight in subspecies of mice. Exp Anim 48, 277-283.
41. Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185-199.
42. Leamy L (1982a) Morphometric studies in inbred and hybrid house mice II. Patterns in the variances. J Hered 73, 267-272.
43. Leamy L (1982b) Morphometric studies in inbred and hybrid house mice. I. Patterns in the mean values. J Hered 73, 171-176.
44. Leamy LJ, Routman EJ, Cheverud JM (1999) Quantitative trait loci for early-and late-developing skull characters in mice: a test of the genetic independence model of morphological integration. Am Nat 153, 201-214.
45. Leamy L, Klingenberg C, Sherratt E, et al. (2008) A search for quantitative trait loci exhibiting imprinting effects on mouse mandible size and shape. Heredity 101, 518-526.
46. Lele S, Richtsmeier JT (1991) Euclidean distance matrix analysis: a coordinate-free approach for comparing biological shapes using landmark data. Am J Phys Anthropol 86, 415-427.
47. Lenarcic AB, Svenson KL, Churchill GA, et al. (2012) A general Bayesian approach to analyzing diallel crosses of inbred strains. Genetics 190, 413-435.
48. Lieberman DE, Ross CF, Ravosa MJ (2000) The primate cranial base: ontogeny, function, and integration. Am J Phys Anthropol 113(Suppl. 31), 117-169.
49. Liu F, van der Lijn F, Schurmann C, et al. (2012) A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 8, e1002932.
50. Macholan M (1996) Morphometric analysis of European house mice. Acta Theriol 41, 255-276.
51. Macholán M, Mikula O, Vohralík V (2008) Geographic phenetic variation of two eastern-Mediterranean non-commensal mouse species, Mus macedonicus and M. cypriacus (Rodentia: Muridae) based on traditional and geometric approaches to morphometrics. Zool Anz -A J Comp Zool 247, 67-80.
52. Martínez-Abadías N, Esparza M, Sjøvold T, et al. (2009) Heritability of human cranial dimensions: comparing the evolvability of different cranial regions. J Anat 214, 19-35.
53. Martínez-Abadías N, Percival C, Aldridge K, et al. (2010) Beyond the closed suture in Apert mouse models: evidence of primary effects of FGFR2 signaling on facial shape at P0. Dev Dyn 239, 3058-3071.
54. Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18, 281-292.
55. Nelson RM, Pettersson ME, Carlborg Ö (2013) A century after Fisher: time for a new paradigm in quantitative genetics. Trends Genet 29, 669-676.
56. Pallares LF, Harr B, Turner LM, et al. (2014) Use of a natural hybrid zone for genomewide association mapping of craniofacial traits in the house mouse. Mol Ecol 23, 5756-5770.
57. Paternoster L, Zhurov AI, Toma AM, et al. (2012) Genome-wide association study of three-dimensional facial morphology identifies a variant in PAX3 associated with nasion position. Am J Hum Genet 90, 478-485.
58. Phillippi J, Xie Y, Miller DR, et al. (2014) Using the emerging Collaborative Cross to probe the immune system. Genes Immun 15, 38-46.
59. R Developmental Core Team (2008) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing, Available from: http://www.R-project.org.
60. Richtsmeier JT, McGrath JW (1986) Quantitative genetics of cranial nonmetric traits in randombred mice: heritability and etiology. Am J Phys Anthropol 69, 51-58.
61. Roseman CC, Willmore KE, Rogers J, et al. (2010) Genetic and environmental contributions to variation in baboon cranial morphology. Am J Phys Anthropol 143, 1-12.
62. Schoenebeck JJ, Ostrander EA (2013) The genetics of canine skull shape variation. Genetics 193, 317-325.
63. Schoenebeck JJ, Hutchinson SA, Byers A, et al. (2012) Variation of BMP3 contributes to dog breed skull diversity. PLoS Genet 8, e1002849.
64. Sherwood RJ, Duren DL, Demerath EW, et al. (2008a) Quantitative genetics of modern human cranial variation. J Hum Evol 54, 909.
65. Sherwood RJ, Duren DL, Havill LM, et al. (2008b) A genomewide linkage scan for quantitative trait loci influencing the craniofacial complex in baboons (Papio hamadryas spp.). Genetics 180, 619-628.
66. Szabo-Rogers HL, Geetha-Loganathan P, Nimmagadda S, et al. (2008) FGF signals from the nasal pit are necessary for normal facial morphogenesis. Dev Biol 318, 289-302.
67. Szabo-Rogers HL, Smithers LE, Yakob W, et al. (2010) New directions in craniofacial morphogenesis. Dev Biol 341, 84-94.
68. Welsh CE, Miller DR, Manly KF, et al. (2012) Status and access to the Collaborative Cross population. Mamm Genome 23, 706-712.
69. Wu P, Jiang T-X, Suksaweang S, et al. (2004) Molecular shaping of the beak. Science 305, 1465-1466.
70. Wu P, Jiang T-X, Shen J-Y, et al. (2006) Morphoregulation of avian beaks: comparative mapping of growth zone activities and morphological evolution. Dev Dyn 235, 1400-1412.
71. Yang H, Wang JR, Didion JP, et al. (2011) Subspecific origin and haplotype diversity in the laboratory mouse. Nat Genet 43, 648-655.
72. Young NM, Chong HJ, Hu D, et al. (2010) Quantitative analyses link modulation of sonic hedgehog signaling to continuous variation in facial growth and shape. Development 137, 3405-3409.
73. Zelditch ML, Bookstein FL, Lundrigan BL (1992) Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46, 1164-1180.