Mapping stem cell activities in the feather follicle

Birds can produce feathers in a remarkable array of shapes, sizes and colours, from undifferentiated precursor cells. A mechanism that might help explain how such diversity is achieved has been identified in a study of the flight feathers of chickens. Three types of stem cells are present, and they migrate to specific positions in the feather follicle. It may be this physical rearrangement that dictates the different morphologies and orientations of the fully fledged feather. This type of distribution of stem cells contrasts to that seen in hair follicles, but in other ways the feather stem cells resemble those of the hair follicle, supporting the idea that feathers and hair arose independently from similar structures around 200 million years ago. It is important to know how different organs ‘manage’ their stem cells. Both hair and feather follicles show robust regenerative powers that episodically renew the epithelial organ. However, the evolution of feathers (from reptiles to birds) and hairs (from reptiles to mammals) are independent events and their follicular structures result from convergent evolution. Because feathers do not have the anatomical equivalent of a hair follicle bulge, we are interested in determining where their stem cells are localized. By applying long-term label retention1, transplantation2 and DiI tracing to map stem cell activities, here we show that feather follicles contain slow-cycling long-term label-retaining cells (LRCs), transient amplifying cells and differentiating keratinocytes. Each population, located in anatomically distinct regions, undergoes dynamic homeostasis during the feather cycle. In the growing follicle, LRCs are enriched in a ‘collar bulge’ niche. In the moulting follicle, LRCs shift to populate a papillar ectoderm niche near the dermal papilla. On transplantation, LRCs show multipotentiality. In a three-dimensional view, LRCs are configured as a ring that is horizontally placed in radially symmetric feathers but tilted in bilaterally symmetric feathers. The changing topology of stem cell activities may contribute to the construction of complex feather forms.