Melanism in Lepidoptera, either industrial or in mimicry, is one of the most commonly cited examples of natural selection [1] [2]. Despite extensive studies of the frequency and maintenance of melanic genes in insect populations [1] [2], there has been little work on the underlying molecular mechanisms. Nowhere is butterfly melanism more striking than in the Eastern Tiger Swallowtail (Papilio glaucus) of North America [3] [4] [5]. In this species, females can be either yellow (wild type) or black (melanic). The melanic form is a Batesian mimic of the distasteful Pipevine Swallowtail (Battus philenor), which is also black in overall color. Melanism in P. glaucus is controlled by a single Y-linked (female) black gene [6]. Melanic females, therefore, always have melanic daughters. Black melanin replaces the background yellow in melanic females. Here, we show that the key enzyme involved is N-beta-alanyl-dopamine-synthase (BAS), which shunts dopamine from the melanin pathway into the production of the yellow color pigment papiliochrome and also provides products for cuticle sclerotization. In melanic females, this enzyme is suppressed, leading to abnormal melanization of a formerly yellow area, and wing scale maturation is also delayed in the same area. This raises the possibility that either reduced BAS activity itself is preventing scale sclerotization (maturation) or, in contrast, that the delay in scale maturation precludes expression of BAS at the correct stage. Together, these data show how changes in expression of a single gene product could result in multiple wing color phenotypes. The implications for the genetic control of mimicry in other Lepidoptera are discussed.
Color pattern formation was studied in wild-type and melanic swallowtails because of their unique pigment system, the papiliochromes, which are derived from the tyrosine as well as from the tryptophan pathway. In a comparative approach we used females of Papilio glaucus which occur in two phenotypes, either wild-type (yellow and black) or melanic. Pigment synthesis in the developing wings starts with formation of yellow papiliochromes followed later by black melanin. From earlier studies we know that dopamine produced from DOPA by the enzyme dopadecarboxylase (DDC), is a precursor of both black melanin and also of N-beta-alanyldopamine (NBAD) in yellow papiliochrome synthesis. Thus, DDC expression and enzyme activity is required in both types of pigment forming scale cells and occurs in a time and pattern specific manner. However, differential activity of DDC alone can not be sufficient to regulate synthesis of different pigments in differently colored scales. Therefore, we tested the hypothesis whether activity of another enzyme, beta-alanyldopamine synthase (BAS), regulates specifically papiliochrome synthesis. BAS transfers beta-alanine to dopamine to give NBAD a component of yellow papiliochrome. We developed a radio-enzyme-assay of BAS activity in which (14C)-beta-alanine is incubated with dopamine, Mg++-ions and ATP together with wing homogenates containing putative BAS activity. In fact, high BAS activity was measured in yellow wings in concert with a high DDC activity. In contrast, in melanic wings almost no BAS activity was found. From this result it is clear, that papiliochrome synthesis in yellow scales is switched on by BAS shifting dopamine into the papiliochrome pathway and out of the melanin pathway or vice versa.
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