Development of fast motion detectors in insect eyes: The example of the male housefly small target motion detector

Many insects evolved the ability to detect and chase rapidly moving prey or mates, and such behavior often corresponds to the presence of a specialized eye region. The best-studied example is the “small target motion detector” (STMD) of the dorsal-anterior retina of the male housefly (Musca domestica), which allows them to perform female pursuit in full flight. We use this feature of the male housefly eye to gain insight into how new traits and cell types appear during development and evolution. We used scRNAseq to identify differentially expressed genes in male-specific cell types during pupal development. We next used CRISPR targeted gene-knockout, and find that the transcription factors Doublesex (Dsx) and Spineless interact in a positive feedback loop critical for the specification of a new photoreceptor type within the STMD in the R7 position. This novel neuronal type expresses broad-spectrum Rhodopsin1 instead of color-sensitive Rhodopsins, and projects to the lamina neuropil instead of the medulla. Dsx and Ss together downregulate Spalt and upregulate Dve, both known to regulate Rhodopsin expression in Drosophila.

We are now using piggyBac transgenesis to test whether the rest of the eye can be converted to this new fate by expression of Dsx alone or if this requires alternative dorsal-anterior determinants. It will be interesting to study how this new gene regulatory network evolved by looking at Dsx binding sites near target genes, finding the enhancers that drive Dsx expression in the dorsal-anterior eye, and by looking at motion detectors in the eyes of other insects.