Correlations of ultrastructure and pigmentation suggest how genes control development of wing scales of Heliconius butterflies

Abstract

Scanning electron microscopy reveals three morphological categories of wing scales in Heliconius butterflies. Type I, white or yellow scales, possess an obverse membrane between longitudinal ridges and lack conspicuous crossribs. Type II, melanic scales, have ladder-like, regular crossribs supported by trabeculae. Type III, red or brown scales, are characterized by crossribs which feature flutes and a thicker, more angular appearance. In hybrids, whose parents possess type I and Type II scales on the hind wing bar respectively, the "bar shadow" scales which replace the yellow bar appear to be slightly modified version of Type II scales. Spectroscopic analyses reveal that yellow, red, and brown pigments are tryptophan derived 3-hydroxykynurenine, dihydroxanthommatin, and xanthommatin, respectively. White is a structural color expressed when yellow pigment is not present, while red and brown are different oxidation states of xanthommatin. Chromatographic evidence suggests the possibility that unstable forms of pigments in this pathway are maintened by association with peptides in the male Thus, although substantial color variation occurs within scale morphological types, it is chemically trivial. Those observations are supplemented by evidence fromthe literature to develop an hypothesis for the relationship between genes, scale pigmentation, and scale structure. Because of the variety of scale morphology and pigment chemistry within the Lepidoptera, it is not possible to asses the degree to which this scheme for Heliconius wing color patttern constitutes a model for other groups. However, it will be surprising if the Heliconius system described here turns out to be other than a variation on a theme common to all butterflies and moths. Indeed, a similar correlation of color and structure has been described for zygaenid moths (Burgeff andSchneider, 1979). More generally, Heliconius wings may contribute to some of the unsolved problems of the genetics and development of tissue specific ommochrome pigmentation. This is because one can work with scale specific regulation of the pathway on the. wings within species having distinctively patterned genotypic varieties or races, rather than rely on constitutive mutants