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

Abstract

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.

The differentiation and morphogenesis of craniofacial muscles

“…The crest-mesoderm interface is undetectable in normal embryos, but is easily identified in chimeric quail-chick/quail-duck embryos (Noden, 1978(Noden, , 1983aHelms and Schneider, 2003;Eames and Schneider, 2005) or mouse embryos in which crest cells are labeled (Jiang et al, 2002;Matsuoka et al, 2005;O'Gormon, 2005). The processes driving movements of tightly condensed EOM primordia remain enigmatic.…”

Developmental stages of the Japanese quail

“…This work has particular impact on the stem cell and reparative fields as feathers demonstrate excellent regenerative abilities and a common precursor cell population is able to produce a diversity of feather morphologies and pigmentation patterns. Much of this work has utilized chick-quail or quail-duck chimeras and therefore it is important that the 'normal' patterns of feather development and pigmentation be recorded (Richardson et al 1990;Eames & Schneider, 2005;Yue et al 2005). …”

Assessing Species-specific Contributions To Craniofacial Development Using Quail-duck Chimeras

“…Interactions between the donor neural crest cells and surrounding host-derived tissues that underlie proper histogenesis and morphogenesis of the craniofacial complex have previously been extensively studied. In particular, neural crest mesenchyme directs species-specific morphology of the face 7,13,51,59 , feather pattern 52 , muscle pattern 56 , and cartilage 53,57 through the regulation of host gene expression. For example, neural crest mesenchyme dictates when bone forms in the mandible by temporally regulating Bmp4 expression 55 .…”