Satb2, modularity, and the evolvability of the vertebrate jaw

Modularity is a key mechanism bridging development and evolution and is fundamental to evolvability. Herein, we investigate modularity of the Vertebrate jaw with the aim of understanding mechanisms of its morphological evolution. Conservation of the basic structural bauplan of Vertebrate jaws led to a Hinge and Caps model, in which polarity in the patterning system of developing jaws predicts modularity. We have tested the hypothesis that the Satb2+ cell population delineates a developmental module within the mandibular jaw. Satb2 is expressed in the mesenchyme of the jaw primordia that gives rise to distal elements of both the upper and lower jaws. Loss of Satb2 specifically affects structural elements of the distal (incisor) domain, reflecting the integration of these elements as well as their independence from other mandibular domains. Reducing Satb2 dosage leads to an increase in variation in mandibular length, providing insight into the developmental potential to generate variation. Inter‐taxa comparisons reveal that the Satb2 domain is conserved within gnathostomes. We complement previous loss of function studies in mice with gene knock‐down experiments in Xenopus, providing evidence for functional conservation of Satb2 in regulating size. Finally, we present evidence that the relative size of the amniote mandibular Satb2+ domain varies in relation to epithelial Fgf8 expression, suggesting a mechanism for evolutionary change in this domain. Taken together, our data support the Hinge and Caps model and provide evidence that Satb2 regulates coordinated distal jaw modules that are subject to evolutionary modification by signals emanating from the Hinge.

[1]  G. ELLIOT SMITH,et al.  Studies on the Structure and Development of Vertebrates , 1930, Nature.

[2]  Sir,et al.  The Development of the Vertebrate Skull , 1938, Nature.

[3]  C. Waddington,et al.  Selection for developmental canalisation. , 1966, Genetical research.

[4]  W. J. Moore The Mammalian Skull , 1981 .

[5]  J. Cheverud PHENOTYPIC, GENETIC, AND ENVIRONMENTAL MORPHOLOGICAL INTEGRATION IN THE CRANIUM , 1982, Evolution; international journal of organic evolution.

[6]  Larry J. Leamy,et al.  Morphometric Studies in Inbred and Hybrid House Mice. V. Directional and Fluctuating Asymmetry , 1984, The American Naturalist.

[7]  L. Leamy Morphometric studies in inbred and hybrid house mice. VI. A genetical analysis of brain and body size , 1985, Behavior genetics.

[8]  W. Atchley,et al.  Genetics of mandible form in the mouse. , 1985, Genetics.

[9]  J. Cheverud,et al.  A COMPARISON OF GENETIC AND PHENOTYPIC CORRELATIONS , 1988, Evolution; international journal of organic evolution.

[10]  J. Richtsmeier,et al.  A quantitative genetic analysis of localized morphology in mandibles of inbred mice using finite element scaling analysis. , 1991, Journal of craniofacial genetics and developmental biology.

[11]  W. Atchley,et al.  A MODEL FOR DEVELOPMENT AND EVOLUTION OF COMPLEX MORPHOLOGICAL STRUCTURES , 1991, Biological reviews of the Cambridge Philosophical Society.

[12]  H. Weintraub,et al.  Xenopus embryos regulate the nuclear localization of XMyoD. , 1994, Genes & development.

[13]  Günter P. Wagner,et al.  Adaptation and the Modular Design of Organisms , 1995, ECAL.

[14]  J. Cheverud Morphological Integration in the Saddle-Back Tamarin (Saguinus fuscicollis) Cranium , 1995, The American Naturalist.

[15]  David Ish-Horowicz,et al.  Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta , 1995, Nature.

[16]  G. Wagner HOMOLOGUES, NATURAL KINDS AND THE EVOLUTION OF MODULARITY , 1996 .

[17]  R. Raff Understanding Evolution: The Next Step. (Book Reviews: The Shape of Life. Genes, Development, and the Evolution of Animal Form.) , 1996 .

[18]  J. Cheverud Developmental Integration and the Evolution of Pleiotropy , 1996 .

[19]  G. Wagner,et al.  A POPULATION GENETIC THEORY OF CANALIZATION , 1997, Evolution; international journal of organic evolution.

[20]  R. Balling,et al.  Antagonistic Interactions between FGF and BMP Signaling Pathways: A Mechanism for Positioning the Sites of Tooth Formation , 1997, Cell.

[21]  G Wagner,et al.  Complexity matters , 1998, Nature Physics.

[22]  P. O'higgins,et al.  Facial growth in Cercocebus torquatus: an application of three‐dimensional geometric morphometric techniques to the study of morphological variation , 1998, Journal of anatomy.

[23]  H. Nijhout,et al.  GENETICS OF FLUCTUATING ASYMMETRY: A DEVELOPMENTAL MODEL OF DEVELOPMENTAL INSTABILITY , 1999, Evolution; international journal of organic evolution.

[24]  M. Depew,et al.  Dlx5 regulates regional development of the branchial arches and sensory capsules. , 1999, Development.

[25]  B. Hall The Neural Crest in Development and Evolution , 2013, Springer New York.

[26]  M. Depew,et al.  Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. , 1999, Genes & development.

[27]  R. Raff,et al.  Dissociability, modularity, evolvability , 2000, Evolution & development.

[28]  P. Sharpe,et al.  Temporospatial cell interactions regulating mandibular and maxillary arch patterning. , 2000, Development.

[29]  B. Hall,et al.  Altered timing of the extracellular-matrix-mediated epithelial-mesenchymal interaction that initiates mandibular skeletogenesis in three inbred strains of mice: development, heterochrony, and evolutionary change in morphology. , 2001, The Journal of experimental zoology.

[30]  Thomas Lufkin,et al.  Specification of Jaw Subdivisions by Dlx Genes , 2002, Science.

[31]  LANDEl,et al.  THE GENETIC COVARIANCE BETWEEN CHARACTERS MAINTAINED BY PLEIOTROPIC MUTATIONS , 2003 .

[32]  Christian Peter Klingenberg,et al.  Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? , 2003, Evolution & development.

[33]  A. Graham,et al.  The neural crest , 2003, Current Biology.

[34]  B. Hall Unlocking the Black Box between Genotype and Phenotype: Cell Condensations as Morphogenetic (modular) Units , 2003 .

[35]  R. Grosschedl,et al.  SUMO modification of a novel MAR-binding protein, SATB2, modulates immunoglobulin mu gene expression. , 2003, Genes & development.

[36]  S. Kuratani Evolution of the vertebrate jaw: homology and developmental constraints , 2003 .

[37]  D. Bonthron,et al.  Identification of SATB2 as the cleft palate gene on 2q32-q33. , 2003, Human molecular genetics.

[38]  C. Kimmel,et al.  Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint , 2003, Development.

[39]  S. Kuratani Evolution of the vertebrate jaw: comparative embryology and molecular developmental biology reveal the factors behind evolutionary novelty , 2004, Journal of anatomy.

[40]  A Population of , 2004 .

[41]  G. Yamada,et al.  Bapx1 regulates patterning in the middle ear: altered regulatory role in the transition from the proximal jaw during vertebrate evolution , 2004, Development.

[42]  J. Vermeesch,et al.  The del(2)(q32.2q33) deletion syndrome defined by clinical and molecular characterization of four patients. , 2005, European journal of medical genetics.

[43]  C. Klingenberg Developmental constraints, modules, and evolvability , 2005 .

[44]  T. Flatt The Evolutionary Genetics of Canalization , 2005, The Quarterly Review of Biology.

[45]  M. Depew,et al.  Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development , 2005, Journal of anatomy.

[46]  S. Kuratani Developmental studies of the lamprey and hierarchical evolutionary steps towards the acquisition of the jaw , 2005, Journal of anatomy.

[47]  O. Britanova,et al.  Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue‐specific manner and demonstrates cell‐type‐dependent expression in the developing mouse CNS , 2005, The European journal of neuroscience.

[48]  M. Bei,et al.  Modification of Msx1 by SUMO-1. , 2006, Biochemical and biophysical research communications.

[49]  Jennifer J. Lund,et al.  SUMO1 Haploinsufficiency Leads to Cleft Lip and Palate , 2006, Science.

[50]  O. Britanova,et al.  Satb2 haploinsufficiency phenocopies 2q32-q33 deletions, whereas loss suggests a fundamental role in the coordination of jaw development. , 2006, American journal of human genetics.

[51]  M. Depew,et al.  21st Century neontology and the comparative development of the vertebrate skull , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[52]  I. Fariñas,et al.  SATB2 Is a Multifunctional Determinant of Craniofacial Patterning and Osteoblast Differentiation , 2006, Cell.

[53]  G. Wagner,et al.  The road to modularity , 2007, Nature Reviews Genetics.

[54]  Philip Stanier,et al.  FGF signalling and SUMO modification: new players in the aetiology of cleft lip and/or palate. , 2007, Trends in genetics : TIG.

[55]  B. Hallgrímsson,et al.  Evolvability as the proper focus of evolutionary developmental biology , 2007, Evolution & development.

[56]  J. Brosens,et al.  TBX22 missense mutations found in patients with X-linked cleft palate affect DNA binding, sumoylation, and transcriptional repression. , 2007, American journal of human genetics.

[57]  Tayard Desudchit,et al.  Heterozygous nonsense mutation SATB2 associated with cleft palate, osteoporosis, and cognitive defects , 2007, Human mutation.

[58]  C. Compagnucci,et al.  Tweaking the hinge and caps: testing a model of the organization of jaws. , 2008, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[59]  Aaron R. Wood,et al.  Building Developmental Integration into Functional Systems: Function-Induced Integration of Mandibular Shape , 2009, Evolutionary Biology.

[60]  Aaron R. Wood,et al.  Modularity of the rodent mandible: Integrating bones, muscles, and teeth , 2008, Evolution & development.

[61]  M. Depew Analysis of skeletal ontogenesis through differential staining of bone and cartilage. , 2008, Methods in molecular biology.

[62]  Trish E. Parsons,et al.  Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation , 2009, Evolutionary Biology.

[63]  Leslie G. Valiant,et al.  Evolvability , 2009, JACM.

[64]  M. Dixon,et al.  A cross‐species analysis of Satb2 expression suggests deep conservation across vertebrate lineages , 2010, Developmental dynamics : an official publication of the American Association of Anatomists.

[65]  Meredith V. Trotter,et al.  Robustness and evolvability. , 2010, Trends in genetics : TIG.

[66]  Hae-Chul Park,et al.  The expression profile and function of Satb2 in zebrafish embryonic development , 2010, Molecules and cells.

[67]  S. Kuraku,et al.  Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. , 2010, Developmental biology.