METHODS, MODELS, METAPHORICAL AIDS

Background

Scale vs. Pattern-level control in development

Heliconius wing as a computer screen

Regulatory Genes and Computer Screens

In order to illustrate what happens on a Heliconius wing while maintaining the computer analogy, it is necessary to mimic the way developmental compartments (windows) might organize expression of pattern genes on real wings. For simplicity imagine proximal and distal, dorsal and ventral compartments on forewing and hindwing. This requires eight windows, one to represent a "compartment" in each of eight wing sectors. Each window is uniquely associated with a different set of applications, representing the regulatory genes that are constrained by compartments in the developing wing. To open any image file and display a pattern in the appropriate window, the appropriate application must first be opened.

An intuitive case to which this model probably applies is the FW of H. melpomene. A quick examination of dorsal and ventral surfaces of some H. melpomene races leaves no doubt that the dorsal and ventral (D/V) surfaces of Heliconius wings represent strikingly different realms of regulatory gene activity, if not compartments (see below). The Central American race, rosina, possesses red (type III) scales in a narrow band distal to the median on the FW dorsal surface (best seen in Figure 1 f). However, differentiation in the same pattern region on the ventral surface is separately controlled and consists of white (type I) scales, a juxtaposition which accounts for the bright, rose-pink color of the wing (personal observation). Therefore the realizator gene that creates red scales in the distal part of the Heliconius melpomene/cydno dorsal FW ("Window 1"), does so after interpreting information provided by appropriate regulatory (homeotic?) genes, (i.e., the selector genes in Garcia-Bellido's model, or "application" in the computer metaphor) which in turn are constrained by compartment boundaries (the window's frame). Thus, only inside the compartment on the dorsal wing does the realizator for "all red" express after receiving signals from appropriate selector genes. Meanwhile on the ventral FW ("Window 2"), red scales do not appear in the homologous area because the appropriate selectors are not active in that particular compartment. Thus in terms of the computer screen metaphor, Window 2, representing a ventral compartment of the distal FW, contains the image file that would specify an all-red (type III) pixel image in the applicationšs window, but that cannot be opened (leaving default, type I pixels in that area), while it can be opened and displayed within the bounds of Window 1, which represents a compartment on the distal part of the dorsal FW. (see also Figure 2 a and b and genetic discussion below.)

If, during development, a somatic mutation in the appropriate homeotic gene occurs, realizator genes normally expressed on another wing surface can be expressed in any scales derived clonally from the original mutant cell. Such "exotic" clones are cell-autonomous in that their differentiation proceeds independently of adjacent "native" cells. Such homeotic mutations, or their phenocopies, can result in patterns of one wing surface appearing as a mosaic patch within a novel region. This phenomenon, known as homeosis, has been reviewed and analyzed for the Lepidoptera by Sibatani (1980). Although D/V homeosis is not known in Drosophila (making the hypothesis of D/V compartments suspect), it has been diagnosed in butterflies such as lycaenids in which scale types can differ strikingly between dorsal and ventral FW surfaces (Sibatani 1980).

The size of such a mosaic patch is a function of how early the causal somatic mutation occurred. Likewise certain developmental boundaries, established prior to the origin of the homeotic mutant clone, may constrain its distribution on the wing, an observation that originally led to the compartment concept in other insects. My observations of spontaneous homeosis in Heliconius (Gilbert in prep.) demonstrates cell autonomous differentiation of scales with respect to scale type and color (e.g., Figure 3a). Likewise experimental induction of somatic mutations in Heliconius embryos which generally reflect phenomena known from clonal analysis of Drosophila imaginal discs (Nöthiger 1981), also indicate cell autonomous differentiation of scale types and suggest that determination of some major pattern boundaries on the wing may occur very early in development (e.g., Figure 3b). No other similar work from butterflies is available for comparison.