Error message

No crossref credentials set for develop

Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development

Development, 1 April 2005
Vol. 132, Issue 7, p. 1499-1509
DOI: 10.1242/dev.01719

Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development

  1. B. Frank Eames and
  2. Richard A. Schneider*
  1. Department of Orthopaedic Surgery, University of California at San Francisco, 533 Parnassus Avenue, U-453, San Francisco, CA 94143-0514, USA
  1. * Author for correspondence (e-mail: ras{at}itsa.ucsf.edu)

Summary

The avian feather complex represents a vivid example of how a developmental module composed of highly integrated molecular and histogenic programs can become rapidly elaborated during the course of evolution. Mechanisms that facilitate this evolutionary diversification may involve the maintenance of plasticity in developmental processes that underlie feather morphogenesis. Feathers arise as discrete buds of mesenchyme and epithelium, which are two embryonic tissues that respectively form dermis and epidermis of the integument. Epithelial-mesenchymal signaling interactions generate feather buds that are neatly arrayed in space and time. The dermis provides spatiotemporal patterning information to the epidermis but precise cellular and molecular mechanisms for generating species-specific differences in feather pattern remain obscure. In the present study, we exploit the quail-duck chimeric system to test the extent to which the dermis regulates the expression of genes required for feather development. Quail and duck have distinct feather patterns and divergent growth rates, and we exchange pre-migratory neural crest cells destined to form the craniofacial dermis between them. We find that donor dermis induces host epidermis to form feather buds according to the spatial pattern and timetable of the donor species by altering the expression of members and targets of the Bone Morphogenetic Protein, Sonic Hedgehog and Delta/Notch pathways. Overall, we demonstrate that there is a great deal of spatiotemporal plasticity inherent in the molecular and histogenic programs of feather development, a property that may have played a generative and regulatory role throughout the evolution of birds.

  • Feather morphogenesis
  • Quail-duck chimeras
  • Neural crest transplants
  • Epithelial-mesenchymal interactions
  • Modularity
  • Plasticity
  • Evolutionary developmental biology
  • bmp4
  • bmp2
  • shh
  • delta

Footnotes

    • Accepted January 31, 2005.

Citation:

B. F. Eames and R. A. Schneider, Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development. Development 132, 1499-1509 (2005).

Multiple developmental mechanisms regulate species-specific jaw size
J. L. Fish, R. S. Sklar, K. C. Woronowicz, and R. A. Schneider
Development 141, 674-684 (1 February 2014)

A simple PCR-based strategy for estimating species-specific contributions in chimeras and xenografts
E. L. Ealba, and R. A. Schneider
Development 140, 3062-3068 (15 July 2013)

Role of canonical Wnt signaling/{beta}-catenin via Dermo1 in cranial dermal cell development
T. H. Tran, A. Jarrell, G. E. Zentner, A. Welsh, I. Brownell, P. C. Scacheri, and R. Atit
Development 137, 3973-3984 (1 December 2010)

Development of the pseudothumb in frogs
M. Tokita, and N. Iwai
Biol Lett 6, 517-520 (23 August 2010)

The Cells that Fill the Bill: Neural Crest and the Evolution of Craniofacial Development
A. H. Jheon, and R. A. Schneider
JDR 88, 12-21 (1 January 2009)

The genesis of cartilage size and shape during development and evolution
B. F. Eames, and R. A. Schneider
Development 135, 3947-3958 (1 December 2008)

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
Development 135, 1223-1234 (1 April 2008)

Developmental evolution of sexual ornamentation: model and a test of feather growth and pigmentation
A. V. Badyaev, and E. A. Landeen
Integr. Comp. Biol. 47, 221-233 (1 August 2007)

Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis
F. Santagati, M. Minoux, S.-Y. Ren, and F. M. Rijli
Development 132, 4927-4936 (15 November 2005)

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882