Sexually monomorphic wing pigmentation pattern does not contribute to mate choice in Drosophila guttifera

In many animal groups, sexually dimorphic ornaments are thought to be evolved by intraspecific competition or mate choice. Some researchers pointed out that sexually monomorphic ornaments could also be evolved by mate choice by both sexes or either sex. Many species of fruit fly have sexually monomorphic wing pigmentation. However, involvement of their sexually monomorphic ornaments in mate choice has not been tested. We aimed to examine whether the sexually monomorphic polka-dotted pattern on wings of Drosophila guttifera contributes to mate choice. Because D. guttifera does not mate in the dark condition at all and courtship sound was not observed, some visual information is likely to be used in mating behaviour. We compared the number of mates between individuals with and without wings, and found that presence of wings influenced mate choice in both sexes. We then compared the number of mates between individuals bearing replaced wings, one group for conspecific D. guttifera wings and another group for heterospecific D. melanogaster wings with no pigmentation pattern. The effect of conspecific/heterospecific wings was only detected in mate choice by females. By comparison between wild-type and black-painted wings, we found no evidence of contribution of wing pigmentation pattern to mate choice in either sex.

Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

How evolutionary novelties have arisen is one of the central questions in evolutionary biology. Pre-existing gene regulatory networks or signaling pathways have been shown to be co-opted for building novel traits in several organisms. However, the structure of entire gene regulatory networks and evolutionary events of gene co-option for emergence of a novel trait are poorly understood. In this study, we used a novel wing pigmentation pattern of the polka-dotted fruit fly, and identified the complete set of genes for pigmentation pattern formation by de novo genome sequencing and transcriptome analyses. In pigmentation areas of wings, 151 genes were positively or negatively regulated by wingless, a master regulator of wing pigmentation. Genes for neural development, Wnt signaling, Dpp signaling, Zinc finger transcription factors, and effectors (such as enzymes) for melanin pigmentation were included among these 151 genes. None of the known regulatory genes that regulate pigmentation pattern formation in other fruit fly species were included. Our results suggest that the novel pigmentation pattern of the polka-dotted fruit fly emerged through multi-step co-options of multiple gene regulatory networks, signaling pathways, and effector genes, rather than recruitment of one large gene circuit.

Co-evolving wing spots and mating displays are genetically separable traits in Drosophila

The evolution of sexual traits often involves correlated changes in morphology and behavior. For example, in Drosophila, divergent mating displays are often accompanied by divergent pigment patterns. To better understand how such traits co-evolve, we investigated the genetic basis of correlated divergence in wing pigmentation and mating display between the sibling species Drosophila elegans and D. gunungcola. Drosophila elegans males have an area of black pigment on their wings known as a wing spot and appear to display this spot to females by extending their wings laterally during courtship. By contrast, D. gunungcola lacks both of these traits. Using Multiplexed Shotgun Genotyping (MSG), we identified a ∼440 kb region on the X chromosome that behaves like a genetic switch controlling the presence or absence of male-specific wing spots. This region includes the candidate gene optomotor-blind (omb), which plays a critical role in patterning the Drosophila wing. The genetic basis of divergent wing display is more complex, with at least two loci on the X chromosome and two loci on autosomes contributing to its evolution. Introgressing the X-linked region affecting wing spot development from D. gunungcola into D. elegans reduced pigmentation in the wing spots but did not affect the wing display, indicating that these are genetically separable traits. Consistent with this observation, broader sampling of wild D. gunungcola populations confirmed the wing spot and wing display are evolving independently: some D. gunungcola males preformed wing displays similar to D. elegans despite lacking wing spots. These data suggest that correlated selection pressures rather than physical linkage or pleiotropy are responsible for the coevolution of these morphological and behavioral traits. They also suggest that the change in morphology evolved prior to the change in behavior.