Anatomical Science International

, Volume 85, Issue 2, pp 79–91 | Cite as

Ultrastructure of the feather follicle in relation to the formation of the rachis in pennaceous feathers

Original Article

Abstract

The present ultrastructural study on follicle of regenerating feathers of four different avian species focuses on the formation and cytology of the rachis. Epithelial cells within the bottom part of the follicle (the collar) are contacted from mesenchymal cells of the dermal papilla. The most basal part of the collar is formed by a circular epithelium containing germinal cells, while in the upper ramogenic part of the collar barb ridges are generated. Epithelial cells rest upon a basement membrane that is stretched in actively forming barb ridges among which anchored mesenchymal cells send thin elongation. This observation suggests that an intense exchange of molecules with the epithelium occurs. The process of formation of the rachis occurs by fusion of barb ridges with the nonsegmented, dorsal or anterior part of the collar. The latter becomes the rachidial ridge, the upper part of the collar where barbs form the branches of the pennaceous feather. The rachis grows and matures into an external cortical part, containing compact corneous material (feather keratin, as confirmed by immunocytochemistry), and a vacuolated medulla with a process similar to that occurring in rami of single barbs. The extension of the medulla and cortex varies along the rachis in different species. In general a thin cortex is formed in those sections of the rachis where barbs are absent, and the feather keratin positive layer increases in the basal part of the feather, the calamus.

Keywords

Regenerating feathers Follicle epithelium Mesenchyme Rachis Ultrastructure 

References

  1. Alibardi L (2005a) Cell structure of developing barbs and barbules in downfeathers of the chick: central role of barb ridge morphogenesis for the evolution of feathers. J Submicrosc Cytol Pathol 37:19–41PubMedGoogle Scholar
  2. Alibardi L (2005b) Fine structure of juvenile feathers of the zebrafinch in relation to the evolution and diversification of pennaceous feathers. J Submicrosc Cytol Pathol 37:323–343PubMedGoogle Scholar
  3. Alibardi L (2006a) Cell structure of barb ridges in down feathers and juvenile feathers of the developing chick embryo: barb ridge modification in relation to feather evolution. Ann Anat 188:303–318CrossRefPubMedGoogle Scholar
  4. Alibardi L (2006b) Cells of embryonic and regenerating germinal layers within barb ridges: implication for the development, evolution and diversification of feathers. J Submicrosc Cytol Pathol 38:51–76PubMedGoogle Scholar
  5. Alibardi L (2007a) Cell organization of barb ridges in regenerating feathers of the quail: implications of the elongation of barb ridges for the evolution and diversification of feathers. Acta Zool 88:101–117CrossRefGoogle Scholar
  6. Alibardi L (2007b) Wedge cells during regeneration of juvenile and adult feathers and their role in carving out the branching pattern of barbs. Ann Anat 189:234–242CrossRefPubMedGoogle Scholar
  7. Alibardi L (2007c) Cell interactions in barb ridges of developing chick downfeather and the origin of the feather branching. Ital J Zool 74:143–155CrossRefGoogle Scholar
  8. Alibardi L (2007d) Cytological aspects of the differentiation of barb cells during the formation of the ramus of feathers. Int J Morphol 25:73–83CrossRefGoogle Scholar
  9. Alibardi L (2007e) Keratinization of sheath and calamus cells in developing and regenerating feathers. Ann Anat 189:583–595CrossRefPubMedGoogle Scholar
  10. Alibardi L (2009a) Follicular patterns during feather morphogenesis in relation to the formation of asymmetric feathers, filoplumes and bristles. Ital J Zool 76 (in press)Google Scholar
  11. Alibardi L (2009b) Cornification of the pulp epithelium and formation of pulp cups in downfeathers and pennaceous feathers. Anat Sci Int (in press)Google Scholar
  12. Alibardi L, Sawyer RH (2006) Cell structure of developing downfeathers in the zebrafinch with emphasis on barb ridge morphogenesis. J Anat 208:621–642CrossRefPubMedGoogle Scholar
  13. Alibardi L, Knapp LW, Sawyer RH (2006) Beta-keratin localization in developing alligator scales and feathers in relation to the development and evolution of feathers. J Submicrosc Cytol Pathol 38:175–192PubMedGoogle Scholar
  14. Bleiweiss R (1987) Development and evolution of avian racket plumes: fine structure and serial homology of the wire. J Morphol 194:23–39CrossRefGoogle Scholar
  15. Brush AH (1993) The origin of feathers: a novel approach. In: Farner D, King JA, Parker KC (eds) Avian biology, vol IX. Academic, New York, pp 121–162Google Scholar
  16. Chodankar R, Cheng CH, Yue Z, Jiang TX, Suksaweang S, Burrus LW, Chuong CM, Widelitz RB (2002) Shift of localized growth zones contributes to skin appendage morphogenesis: role of the Wnt/-β-catenin pathway. J Investig Dermatol 120:20–26CrossRefGoogle Scholar
  17. Chuong CM (1993) The making of a feather: homeoproteins, retinoids and adhesion molecules. BioEssays 15:513–521CrossRefPubMedGoogle Scholar
  18. Chuong CM, Widelitz RB (1999) Feather morphogenesis: a model of the formation of epithelial appendages. In: Chuong CM (ed) Molecular basis of epithelial appendage morphogenesis. Landes Bioscience, Georgtown, pp 57–73Google Scholar
  19. Chuong MC, Wu P, Zhang FC, Xu X, Yu M, Widelitz RB, Jianf TX, Hour L (2003) Adaptation to the sky: defining the feather with integument fossils from mesozoic china and experimental evidence from molecular laboratories. J Exp Zool 298B:42–56CrossRefGoogle Scholar
  20. Filshie BK, Rogers GE (1962) An electron microscope study of the fine structure of feather keratin. J Cell Biol 13:1–12CrossRefPubMedGoogle Scholar
  21. Gregg K, Rogers GE (1986) Feather keratin: composition, structure and biogenesis. In: Bereiter-Hahn J, Matoltsy AG, Sylvia-Richards K (eds) Biology of the integument, vol 2, vertebrates. Springer, Berlin, pp 666–694Google Scholar
  22. Harris MP, Fallon JF, Prum RO (2002) Shh-Bmp2 signaling module and the evolutionary origin and diversification of feathers. J Exp Zool 294B:160–176CrossRefGoogle Scholar
  23. King JR, Murphy ME (1987) Amino acid composition of the calamus, rachis, and barbs of the white-crowned sparrow feathers. Condor 89:436–439CrossRefGoogle Scholar
  24. Lucas AM, Stettenheim PR (1972) Growth of follicles and feathers. Color of feathers and integument. In “Avian anatomy. Integument”. Agriculture Handbook 362. US Department of Agriculture. Washington, DC, Chap 7, pp 341–419Google Scholar
  25. Maderson PFA, Alibardi L (2000) The development of the sauropsid integument: a contribution to the problem of the origin and evolution of feathers. Am Zool 40:513–529CrossRefGoogle Scholar
  26. Matulionis DH (1970) Morphology of the developing down feathers of chick embryos. A descriptive study at the ultrastructural level of differentiation and keratinization. Z Anat Entw Gesch 132:107–157CrossRefGoogle Scholar
  27. Prum OR (1999) Development and evolutionary origin of feathers. J Exp Zool 285B:291–306CrossRefGoogle Scholar
  28. Prum OR, Dyck J (2003) A hierarchical model of plumage: morphology, development, and evolution. J Exp Zool 298B:73–90CrossRefGoogle Scholar
  29. Prum OR, Williamson S (2001) Theory of the growth and evolution of feather shape. J Exp Zool 291:30–57CrossRefPubMedGoogle Scholar
  30. Sawyer RH, Knapp LW (2003) Avian skin development and the evolutionary origin of feathers. J Exp Zool 298B:57–72CrossRefGoogle Scholar
  31. Sawyer RH, Glenn T, French JO, Mays B, Shames RB, Barnes GL, Rhodes W, Ishikawa Y (2000) The expression of beta keratins in the epidermal appendages of reptiles and birds. Am Zool 40:530–539CrossRefGoogle Scholar
  32. Scala C, Cenacchi G, Ferrari C, Pasquinelli G, Preda P, Manara G (1992) A new acrylic resin formulation: a useful tool for histological, ultrastructural, and immunocytochemical investigation. J Histochem Cytochem 40:1799–1804PubMedGoogle Scholar
  33. Spearman RIC, Hardy JA (1985) Integument. In: King AS, McLelland J (eds) Form and function of birds, vol 3. Academic, London, pp 1–56Google Scholar
  34. Yu M, Yue Z, Wu P, Wu DY, Mayer JA, Medina M, Widelitz RB, Jiang TX, Chuong MC (2004) The developmental biology of feather follicle. Int J Dev Biol 48:181–191CrossRefPubMedGoogle Scholar
  35. Yue Z, Jiang TX, Jiang TX, Jiang TX, Widelitz RB, Yue Z, Jiang Z, Widelitz RB, Chuong CM (2005) Mapping stem cell activities in the feather follicle. Nature 438:1026–1029CrossRefPubMedGoogle Scholar

Copyright information

© Japanese Association of Anatomists 2009

Authors and Affiliations

  1. 1.Dipartimento di Biologia Evoluzionistica SperimentaleUniversity of BolognaBolognaItaly

Personalised recommendations