No abstract

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

The evolutionary trajectories and genetic architectures underlying ecological divergence with gene flow are poorly understood. Sympatric timing types of the intertidal insect Clunio marinus (Diptera) from Roscoff (France) differ in lunar reproductive timing. One type reproduces at full moon, the other at new moon, controlled by a circalunar clock of yet unknown molecular nature. Lunar reproductive timing is a magic trait for a sympatric speciation process, as it is both ecologically relevant and entails assortative mating. Here we show that the difference in reproductive timing is controlled by at least four quantitative trait loci (QTL) on three different chromosomes. They are partly associated with complex inversions, but differentiation of the inversion haplotypes cannot explain the different phenotypes. The most differentiated locus in the entire genome, with QTL support, is the period locus, implying that this gene could not only be involved in circadian timing but also in lunar timing. Our data indicate that magic traits can be based on an oligogenic architecture and can be maintained by selection on several unlinked loci.

The evolutionary trajectories and genetic architectures underlying ecological divergence with gene flow are poorly understood. Sympatric timing types of the intertidal insect Clunio marinus (Diptera) from Roscoff (France) differ in lunar reproductive timing. One type reproduces at full moon, the other at new moon, controlled by a circalunar clock of yet unknown molecular nature. Lunar reproductive timing is a magic trait for a sympatric speciation process, as it is both ecologically relevant and entails assortative mating. Here, we show that the difference in reproductive timing is controlled by at least four quantitative trait loci (QTL) on three different chromosomes. They are partly associated with complex inversions, but differentiation of the inversion haplotypes cannot explain the different phenotypes. The most differentiated locus in the entire genome, with QTL support, is the period locus, implying that this gene could not only be involved in circadian timing but also in lunar timing. Our data indicate that magic traits can be based on an oligogenic architecture and can be maintained by selection on several unlinked loci.

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.