Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Feb 2001; 157(2): 785–802.
PMCID: PMC1461535

Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics.

Abstract

This study introduces a new multivariate approach for analyzing the effects of quantitative trait loci (QTL) on shape and demonstrates this method for the mouse mandible. We quantified size and shape with the methods of geometric morphometrics, based on Procrustes superimposition of five morphological landmarks recorded on each mandible. Interval mapping for F(2) mice originating from an intercross of the LG/J and SM/J inbred strains revealed 12 QTL for size, 25 QTL for shape, and 5 QTL for left-right asymmetry. Multivariate ordination of QTL effects by principal component analysis identified two recurrent features of shape variation, which involved the positions of the coronoid and angular processes relative to each other and to the rest of the mandible. These patterns are reminiscent of the knockout phenotypes of a number of genes involved in mandible development, although only a few of these are possible candidates for QTL in our study. The variation of shape effects among the QTL showed no evidence of clustering into distinct groups, as would be expected from theories of morphological integration. Further, for most QTL, additive and dominance effects on shape were markedly different, implying overdominance for specific features of shape. We conclude that geometric morphometrics offers a promising new approach to address problems at the interface of evolutionary and developmental genetics.

Full Text

The Full Text of this article is available as a PDF (307K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, Mantero S, Bober E, Barbieri O, Simeone A, Levi G. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development. 1999 Sep;126(17):3795–3809. [PubMed]
  • Atchley WR, Hall BK. A model for development and evolution of complex morphological structures. Biol Rev Camb Philos Soc. 1991 May;66(2):101–157. [PubMed]
  • Badyaev AV, Foresman KR. Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proc Biol Sci. 2000 Feb 22;267(1441):371–377. [PMC free article] [PubMed]
  • Bailey DW. Genes that affect the shape of the murine mandible. Congenic strain analysis. J Hered. 1985 Mar-Apr;76(2):107–114. [PubMed]
  • Bailey DW. Genes that affect morphogenesis of the murine mandible. Recombinant-inbred strain analysis. J Hered. 1986 Jan-Feb;77(1):17–25. [PubMed]
  • Birdsall K, Zimmerman E, Teeter K, Gibson G. Genetic variation for the positioning of wing veins in Drosophila melanogaster. Evol Dev. 2000 Jan-Feb;2(1):16–24. [PubMed]
  • Bookstein FL. Biometrics, biomathematics and the morphometric synthesis. Bull Math Biol. 1996 Mar;58(2):313–365. [PubMed]
  • Bünger L, Hill WG. Role of growth hormone in the genetic change of mice divergently selected for body weight and fatness. Genet Res. 1999 Dec;74(3):351–360. [PubMed]
  • Chai CK. Analysis of Quantitative Inheritance of Body Size in Mice. I. Hybridization and Maternal Influence. Genetics. 1956 Mar;41(2):157–164. [PMC free article] [PubMed]
  • Cheverud JM. Quantitative genetics and developmental constraints on evolution by selection. J Theor Biol. 1984 Sep 21;110(2):155–171. [PubMed]
  • Cheverud JM, Hartman SE, Richtsmeier JT, Atchley WR. A quantitative genetic analysis of localized morphology in mandibles of inbred mice using finite element scaling analysis. J Craniofac Genet Dev Biol. 1991 Jul-Sep;11(3):122–137. [PubMed]
  • Cheverud JM, Routman EJ, Duarte FA, van Swinderen B, Cothran K, Perel C. Quantitative trait loci for murine growth. Genetics. 1996 Apr;142(4):1305–1319. [PMC free article] [PubMed]
  • Churchill GA, Doerge RW. Empirical threshold values for quantitative trait mapping. Genetics. 1994 Nov;138(3):963–971. [PMC free article] [PubMed]
  • Debat V, Alibert P, David P, Paradis E, Auffray JC. Independence between developmental stability and canalization in the skull of the house mouse. Proc Biol Sci. 2000 Mar 7;267(1442):423–430. [PMC free article] [PubMed]
  • Leamy LJ, Routman EJ, Cheverud JM. Quantitative trait loci for fluctuating asymmetry of discrete skeletal characters in mice. Heredity (Edinb) 1998 Apr;80(Pt 4):509–518. [PubMed]
  • Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, Pedersen RA, Rubenstein JL. Dlx5 regulates regional development of the branchial arches and sensory capsules. Development. 1999 Sep;126(17):3831–3846. [PubMed]
  • Leamy LJ, Pomp D, Eisen EJ, Cheverud JM. Quantitative trait loci for directional but not fluctuating asymmetry of mandible characters in mice. Genet Res. 2000 Aug;76(1):27–40. [PubMed]
  • Lin CR, Kioussi C, O'Connell S, Briata P, Szeto D, Liu F, Izpisúa-Belmonte JC, Rosenfeld MG. Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature. 1999 Sep 16;401(6750):279–282. [PubMed]
  • Francis-West P, Ladher R, Barlow A, Graveson A. Signalling interactions during facial development. Mech Dev. 1998 Jul;75(1-2):3–28. [PubMed]
  • Gage PJ, Suh H, Camper SA. Dosage requirement of Pitx2 for development of multiple organs. Development. 1999 Oct;126(20):4643–4651. [PubMed]
  • Gilchrist AS, Azevedo RB, Partridge L, O'Higgins P. Adaptation and constraint in the evolution of Drosophila melanogaster wing shape. Evol Dev. 2000 Mar-Apr;2(2):114–124. [PubMed]
  • Lu MF, Cheng HT, Kern MJ, Potter SS, Tran B, Diekwisch TG, Martin JF. prx-1 functions cooperatively with another paired-related homeobox gene, prx-2, to maintain cell fates within the craniofacial mesenchyme. Development. 1999 Feb;126(3):495–504. [PubMed]
  • Goodale HD. PROGRESS REPORT ON POSSIBILITIES IN PROGENY-TEST BREEDING. Science. 1941 Nov 7;94(2445):442–443. [PubMed]
  • Lu MF, Pressman C, Dyer R, Johnson RL, Martin JF. Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature. 1999 Sep 16;401(6750):276–278. [PubMed]
  • Haley CS, Knott SA. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity (Edinb) 1992 Oct;69(4):315–324. [PubMed]
  • Mezey JG, Cheverud JM, Wagner GP. Is the genotype-phenotype map modular? A statistical approach using mouse quantitative trait loci data. Genetics. 2000 Sep;156(1):305–311. [PMC free article] [PubMed]
  • Mo R, Freer AM, Zinyk DL, Crackower MA, Michaud J, Heng HH, Chik KW, Shi XM, Tsui LC, Cheng SH, et al. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development. 1997 Jan;124(1):113–123. [PubMed]
  • Klingenberg CP, Zaklan SD. Morphological intergration between development compartments in the Drosophila wing. Evolution. 2000 Aug;54(4):1273–1285. [PubMed]
  • Rivera-Pérez JA, Mallo M, Gendron-Maguire M, Gridley T, Behringer RR. Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development. 1995 Sep;121(9):3005–3012. [PubMed]
  • Rivera-Pérez JA, Wakamiya M, Behringer RR. Goosecoid acts cell autonomously in mesenchyme-derived tissues during craniofacial development. Development. 1999 Sep;126(17):3811–3821. [PubMed]
  • Lanctôt C, Moreau A, Chamberland M, Tremblay ML, Drouin J. Hindlimb patterning and mandible development require the Ptx1 gene. Development. 1999 May;126(9):1805–1810. [PubMed]
  • Routman E, Cheverud J. A rapid method of scoring simple sequence repeat polymorphisms with agarose gel electrophoresis. Mamm Genome. 1994 Mar;5(3):187–188. [PubMed]
  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA, Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. [PubMed]
  • Routman EJ, Cheverud JM. Polymorphism for PCR-analyzed microsatellites between the inbred mouse strains LG and SM. Mamm Genome. 1995 Jun;6(6):401–404. [PubMed]
  • Laurie CC, True JR, Liu J, Mercer JM. An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana. Genetics. 1997 Feb;145(2):339–348. [PMC free article] [PubMed]
  • Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development. 1997 Jul;124(13):2659–2670. [PMC free article] [PubMed]
  • ten Berge D, Brouwer A, Korving J, Martin JF, Meijlink F. Prx1 and Prx2 in skeletogenesis: roles in the craniofacial region, inner ear and limbs. Development. 1998 Oct;125(19):3831–3842. [PubMed]
  • Weber K, Eisman R, Morey L, Patty A, Sparks J, Tausek M, Zeng ZB. An analysis of polygenes affecting wing shape on chromosome 3 in Drosophila melanogaster. Genetics. 1999 Oct;153(2):773–786. [PMC free article] [PubMed]
  • Zeng ZB, Liu J, Stam LF, Kao CH, Mercer JM, Laurie CC. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics. 2000 Jan;154(1):299–310. [PMC free article] [PubMed]
  • Weber KE. How small are the smallest selectable domains of form? Genetics. 1992 Feb;130(2):345–353. [PMC free article] [PubMed]
  • Zimmerman E, Palsson A, Gibson G. Quantitative trait loci affecting components of wing shape in Drosophila melanogaster. Genetics. 2000 Jun;155(2):671–683. [PMC free article] [PubMed]
  • Whitlock MC, Fowler K. The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics. 1999 May;152(1):345–353. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...