Many ways to make darker flies: Intra- and inter-specific variation in Drosophila body pigmentation components

Abstract

Body pigmentation is an evolutionarily diversified and ecologically relevant trait that shows variation within and between species, and important roles in animal survival and reproduction. Insect pigmentation, in particular, provides some of the most compelling examples of adaptive evolution and its ecological and genetic bases. Yet, while pigmentation includes multiple aspects of color and color pattern that may vary more or less independently, its study frequently focuses on one single aspect. Here, we develop a method to quantify color and color pattern in Drosophila body pigmentation, decomposing thorax and abdominal pigmentation into distinct measurable traits, and we quantify different sources of variation in those traits. For each body part, we measured overall darkness, as well as four other pigmentation properties distinguishing between background color and color of the darker pattern elements that decorate the two body parts. By focusing on two standard D. melanogaster laboratory populations, we show that pigmentation components vary and co-vary in different manners depending on sex, genetic background, and developmental temperature. By studying three natural populations of D. melanogaster along a latitudinal cline and five other Drosophila species, we then show that evolution of lighter or darker bodies can be achieved by changing distinct component traits. Our study underscores the value of detailed phenotyping for a better understanding of phenotypic variation and diversification, and the ecological pressures and genetic mechanisms underlying them.