Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories.

In this special issue on the Evo-Devo of amniote integuments, Alibardi has discussed the adaptation of the integument to the land. Here we will discuss the adaptation to the sky. We first review a series of fossil discoveries representing intermediate forms of feathers or feather-like appendages from dinosaurs and Mesozoic birds from the Jehol Biota of China. We then discuss the molecular and developmental biological experiments using chicken integuments as the model. Feather forms can be modulated using retrovirus mediated gene mis-expression that mimics those found in nature today and in the evolutionary past. The molecular conversions among different types of integument appendages (feather, scale, tooth) are discussed. From this evidence, we recognize that not all organisms with feathers are birds, and that not all skin appendages with hierarchical branches are feathers. We develop a set of criteria for true avian feathers: 1) possessing actively proliferating cells in the proximal follicle for proximo-distal growth mode; 2) forming hierarchical branches of rachis, barbs, and barbules, with barbs formed by differential cell death and bilaterally or radially symmetric; 3) having a follicle structure, with mesenchyme core during development; 4) when mature, consisting of epithelia without mesenchyme core and with two sides of the vane facing the previous basal and supra-basal layers, respectively; and 5) having stem cells and dermal papilla in the follicle and hence the ability to molt and regenerate. A model of feather evolution from feather bud --> barbs --> barbules --> rachis is presented, which is opposite to the old view of scale plate --> rachis --> barbs --> barbules (Regal, '75; Q Rev Biol 50:35).