Propagation of a regular pattern

There are two general assumptions which concern feather patterning. First, that the position of each primordium is determined immediately in advance of morphogenesis in hitherto unpattemed skin. This assumption stands in contrast to

suggests that the site at which organs will form depends on organisation established in the tissue some time before morphogenesis begins (Wolpert, 1971, 1978). Second, the models assume that the repeated, neighbouring units of the pattern are

equivalent. This need not be so, and would not be so were their determination derived from a mechanism based on positional information (Wolpert, 1969; Lewis and Wolpert, 1976).

The particular postulates of the models derive from an examination of the way feather primordia emerge. Since morphogenesis occurs sequentially across the pteryla, it has been suggested that the pattern is propagated row-by-row through the dermis (Ede, 1972; Stuart et al, 1972; Novel, 1973). This view embodies two distinct ideas: first, that some stimulus or permissive condition to form primordia spreads through the dermis immediately in advance of primordium formation; and second, that the regularity of the pattern itself is propagated by a ‘template’ mechanism in which primordia in one row determine the positions of primordia in the next.

Turing (1952) showed how an initially homogeneous system of two or more diffusible and cross-reacting chemical "morphogens" could develop periodic

heterogeneity after small, random disturbances and suggested that such a chemical distribution could form the basis of spacing patterns. Wigglesworth (1940) suggested a model for the regular spacing of bristles in the bug, Rhodnius: that each bristle site, as it formed, utilised precursors from the surrounding tissue and thus, by

competition, inhibited bristle formation within a certain area around it. Claxton (1964) used a similar scheme to account for the pattern of follicles in sheep skin which is of the type exhibited by pelage hairs. Moreover, Claxton (1964) showed

effective inhibition, it is possible to simulate the patterning process and arrive at realistic values for the range and variance of nearest neighbour distances within the pattern.

Ede (1972) proposed the model for feather pattern formation which built on Claxton's approach. According to this model, a zone of inhibition is generated

radially round each forming primordium, by the production of a diffusible substance. New primordia would only form outside a circular threshold contour of inhibition around existing sites. If inhibition decreases steeply across this threshold contour, and some mechanism exists to guarantee primordium formation outside the zone of inhibition, these conditions would give the pattern a well-defined periodicity. To account for the regular array of primordia, Ede assumed the temporal sequence of morphogenesis by suggesting that competence to form primordia is confined to a narrow, but ever-widening band of dermis lateral to already-formed primordia. So, new primordia would form as soon as sufficient competent dermis became available. Ede (1972) suggested that the spread of competent dermis depends on lateral

diffusion o f an activator substance from the midline. However, this would result in an exponential decrease in the rate of initiation of new rows with distance from the midline. In fact, initiation appears to be approximately constant, at least over the first few rows (Hamburger and Hamilton, 1951). This difficulty could be simply overcome by suggesting that the key substance is produced by successive bands of activated dermis. Since the distances between successive rows are small (about 200 to 300 um), the model is plausible in terms of timing (Crick, 1970).

area. The models therefore set out to explain the pattern using space-filling constraints. The geometric regularity of this approach, and the assumption that primordia are equivalent, implies that each new primordium is equidistant from two neighbours in the preceeding row. In all skin appendages, primordia do not form closer together than a certain distance which is characteristic of the pattern; for instance mammalian hair pattern (Claxton, 1964). Moreover, in some patterns where primordia do not form closer together, such as reptilian and avian scale patterns, there is no evidence from histological descriptions that dermal structures are formed which could be expected to interact strictly between primordia (Maderson, 1965; Sawyer, 1972). It can be considered that a different mechanism of pattern

determination may operate in other systems.

Stuart et al, (1972) proposed the following model which is based on one further observation. Histological evidence indicates that between formed primordia, elongated dermal cells are mutually aligned to form 'arrays' (Stuart and Moscona,

1967; Stuart et al., 1972). These arrays intersect at condensations. According to Stuart et al (1972), extracellular fibres are also aligned within these arrays and this arrangement of fibres and cells becomes progressively organised in the dermis lateral to already forming condensations, so that diagono-lateral arrays intersect at the sites of new primordia. The sequence of morphogenesis is accounted for by the

progressive organisation of the dermis into arrays which extend diagono-laterally from formed condensations to generate a lattice of oriented cells and fibres in hitherto unpatterned skin. The intersections in this lattice define the sites of new primordia. Cells move along the fibres in these arrays to intersections where their movement is

do not suggest how the periodic structure of the initial row forms, though they do point out that, in the spinal pteryla, its movement follows the formation of an array along the midline. However, there are some serious difficulties. First, there is

conflicting evidence on whether the arrays actually extend lateral to the most recently formed rows of primordia (Wessell and Evans, 1968) and it is not clear to what extent cells move along fibres in these arrays. Second, the model focuses on features which appear to be unique to the feather system since arrays have not been reported in the superficial dermis in histological accounts of the development of other skin appendages, such as in mouse vibrissae (Wessell and Roessner, 1965) or in chicken or reptilian scales (Maderson 1965; Sawyer, 1972a).

Oster et al (1983) proposed a model based on two properties of mesenchymal cells in vitro. First, cells spread and migrate within a substratum consisting of fibrous extracellular matrix and other cells. Second, motile cells can generate large traction forces on the extracellular matrix. From those two pieces of evidence, Oster et al (1983) showed that the mechanical interaction between the motile cells and their elastic substratum affect the cells’ motion in such a way as to organise spatial patterns. An important cellular behaviour for this consideration is ‘haptotaxis’ which is the directed movement of cells in response to adhesion

gradients in their substratum. This model is focused on the initiation of feather buds and predicts the sequence of bifurcations, leading from a uniform distribution to a columnar array, which then breaks up into isolated aggregations. Subsequent

aggregations spread laterally to form a periodic array. Depending on the anisotropic character of the substratum, the final periodic array can exhibit a variety of