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Science 299 (5606): 565-568

Copyright © 2003 by the American Association for the Advancement of Science

The Cellular and Molecular Origins of Beak Morphology

R. A. Schneider, J. A. Helms*

Cellular and molecular mechanisms underlying differences in beak morphology likely involve interactions among multiple embryonic populations. We exchanged neural crest cells destined to participate in beak morphogenesis between two anatomically distinct species. Quail neural crest cells produced quail beaks in duck hosts and duck neural crest produced duck bills in quail hosts. These transformations involved morphological changes to non-neural crest host beak tissues. To achieve these changes, donor neural crest cells executed autonomous molecular programs and regulated gene expression in adjacent host tissues. Thus, neural crest cells are a source of molecular information that generates interspecific variation in beak morphology.

Department of Orthopaedic Surgery, 533 Parnassus Avenue, Suite U-453, University of California, San Francisco, CA 94143, USA.
*   To whom correspondence should be addressed. E-mail: helms{at}

Multiple developmental mechanisms regulate species-specific jaw size.
J. L. Fish, R. S. Sklar, K. C. Woronowicz, and R. A. Schneider (2014)
Development 141, 674-684
   Abstract »    Full Text »    PDF »
Genomics of a Metamorphic Timing QTL: met1 Maps to a Unique Genomic Position and Regulates Morph and Species-Specific Patterns of Brain Transcription.
R. B. Page, M. A. Boley, D. K. Kump, and S. R. Voss (2013)
Genome Biol Evol 5, 1716-1730
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A simple PCR-based strategy for estimating species-specific contributions in chimeras and xenografts.
E. L. Ealba and R. A. Schneider (2013)
Development 140, 3062-3068
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Human genetic variation within neural crest enhancers: molecular and phenotypic implications.
A. Rada-Iglesias, S. L. Prescott, and J. Wysocka (2013)
Phil Trans R Soc B 368, 20120360
   Abstract »    Full Text »    PDF »
Signals and Switches in Mammalian Neural Crest Cell Differentiation.
S. Bhatt, R. Diaz, and P. A. Trainor (2013)
Cold Spring Harb Perspect Biol 5, a008326
   Abstract »    Full Text »    PDF »
Molecular and cellular changes associated with the evolution of novel jaw muscles in parrots.
M. Tokita, T. Nakayama, R. A. Schneider, and K. Agata (2012)
Proc R Soc B 280, 20122319
   Abstract »    Full Text »    PDF »
Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development.
M. Minoux and F. M. Rijli (2010)
Development 137, 2605-2621
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Comparative gene expression analysis of avian embryonic facial structures reveals new candidates for human craniofacial disorders.
S.A. Brugmann, K.E. Powder, N.M. Young, L.H. Goodnough, S.M. Hahn, A.W. James, J.A. Helms, and M. Lovett (2010)
Hum. Mol. Genet. 19, 920-930
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Novel skeletogenic patterning roles for the olfactory pit.
H. L. Szabo-Rogers, P. Geetha-Loganathan, C. J. Whiting, S. Nimmagadda, K. Fu, and J. M. Richman (2009)
Development 136, 219-229
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The Cells that Fill the Bill: Neural Crest and the Evolution of Craniofacial Development.
A. H. Jheon and R. A. Schneider (2009)
Journal of Dental Research 88, 12-21
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A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm.
D. Hu and R. S. Marcucio (2009)
Development 136, 107-116
   Abstract »    Full Text »    PDF »
The genesis of cartilage size and shape during development and evolution.
B. F. Eames and R. A. Schneider (2008)
Development 135, 3947-3958
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Mesenchyme-dependent BMP signaling directs the timing of mandibular osteogenesis.
A. E. Merrill, B. F. Eames, S. J. Weston, T. Heath, and R. A. Schneider (2008)
Development 135, 1223-1234
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Wnt signaling mediates regional specification in the vertebrate face.
S. A. Brugmann, L. H. Goodnough, A. Gregorieff, P. Leucht, D. ten Berge, C. Fuerer, H. Clevers, R. Nusse, and J. A. Helms (2007)
Development 134, 3283-3295
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The origins of species-specific facial morphology: the proof is in the pigeon.
J. A. Helms and S. A. Brugmann (2007)
Integr. Comp. Biol. 47, 338-342
   Abstract »    Full Text »    PDF »
Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development.
Z. Zhang, T. Huynh, and A. Baldini (2006)
Development 133, 3587-3595
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Early Hedgehog signaling from neural to oral epithelium organizes anterior craniofacial development.
J. K. Eberhart, M. E. Swartz, J. G. Crump, and C. B. Kimmel (2006)
Development 133, 1069-1077
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Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis.
F. Santagati, M. Minoux, S.-Y. Ren, and F. M. Rijli (2005)
Development 132, 4927-4936
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Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development.
B. F. Eames and R. A. Schneider (2005)
Development 132, 1499-1509
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New insights into craniofacial morphogenesis.
J. A. Helms, D. Cordero, and M. D. Tapadia (2005)
Development 132, 851-861
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Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes.
I. K. Quigley, J. M. Turner, R. J. Nuckels, J. L. Manuel, E. H. Budi, E. L. MacDonald, and D. M. Parichy (2004)
Development 131, 6053-6069
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Neural crest cell plasticity and its limits.
N. M. Le Douarin, S. Creuzet, G. Couly, and E. Dupin (2004)
Development 131, 4637-4650
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Bmp4 and Morphological Variation of Beaks in Darwin's Finches.
A. Abzhanov, M. Protas, B. R. Grant, P. R. Grant, and C. J. Tabin (2004)
Science 305, 1462-1465
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Deconstructing the genesis of animal form.
B. Hogan (2004)
Development 131, 2515-2520
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Graded potential of neural crest to form cornea, sensory neurons and cartilage along the rostrocaudal axis.
P. Y. Lwigale, G. W. Conrad, and M. Bronner-Fraser (2004)
Development 131, 1979-1991
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Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development.
S. Creuzet, B. Schuler, G. Couly, and N. M. Le Douarin (2004)
PNAS 101, 4843-4847
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Mesenchymal patterning by Hoxa2 requires blocking Fgf-dependent activation of Ptx1.
N. Bobola, M. Carapuco, S. Ohnemus, B. Kanzler, A. Leibbrandt, A. Neubuser, J. Drouin, and M. Mallo (2003)
Development 130, 3403-3414
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The new mapping.
C. Berry (2003)
QJM 96, 459-460
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A zone of frontonasal ectoderm regulates patterning and growth in the face.
D. Hu, R. S. Marcucio, and J. A. Helms (2003)
Development 130, 1749-1758
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DEVELOPMENT: The Bills of Qucks and Duails.
P. Trainor (2003)
Science 299, 523-524
   Abstract »    Full Text »    PDF »

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