Avian beak diversity is a classic example of morphological evolution. Recently, we showed that localized cell proliferation mediated by bone morphogenetic protein 4 (BMP4) can explain the different shapes of chicken and duck beaks (Wu et al. [2004] Science 305:1465). Here, we compare further growth activities among chicken (conical and slightly curved), duck (straight and long), and cockatiel (highly curved) developing beak primordia. We found differential growth activities among different facial prominences and within one prominence. The duck has a wider frontal nasal mass (FNM), and more sustained fibroblast growth factor 8 activity. The cockatiel has a thicker FNM that grows more vertically and a relatively reduced mandibular prominence. In each prominence the number, size, and position of localized growth zones can vary: it is positioned more rostrally in the duck and more posteriorly in the cockatiel FNM, correlating with beak curvature. BMP4 is enriched in these localized growth zones. When BMP activity is experimentally altered in all prominences, beak size was enlarged or reduced proportionally. When only specific prominences were altered, the prototypic conical shaped chicken beaks were converted into an array of beak shapes mimicking those in nature. These results suggest that the size of beaks can be modulated by the overall activity of the BMP pathway, which mediates the growth. The shape of the beaks can be fine-tuned by localized BMP activity, which mediates the range, level, and duration of locally enhanced growth. Implications of topobiology vs. molecular blueprint concepts in the Evo-Devo of avian beak forms are discussed.

Darwin's theory describes the principles that are responsible for evolutionary change of organisms and their attributes. The actual mechanisms, however, need to be studied for each species and each organ separately. Here we have investigated the mechanisms underlying these principles in the avian feather. Feathers comprise one of the most complex and diverse epidermal organs as demonstrated by their shape, size, patterned arrangement and pigmentation. Variations can occur at several steps along each level of organization, leading to highly diverse forms and functions. Feathers develop gradually during ontogeny through a series of steps that may correspond to the evolutionary steps that were taken during the phylogeny from a reptilian ancestor to birds. These developmental steps include 1) the formation of feather tract fields on the skin surfaces; 2) periodic patterning of the individual feather primordia within the feather tract fields; 3) feather bud morphogenesis establishing anterio -posterior (along the cranio -caudal axis) and proximodistal axes; 4) branching morphogenesis to create the rachis, barbs and barbules within a feather bud; and 5) gradual modulations of these basic morphological parameters within a single feather or across a feather tract. Thus, possibilities for variation in form and function of feathers occur at every developmental step. In this paper, principles guiding feather tract formation, distributions of individual feathers within the tracts and variations in feather forms are discussed at a cellular and molecular level.