Natural genetic variation spans all predicted Rh5/Rh6 expression phenotypes in Drosophila R8 photoreceptors

Standing genetic variation is immediately available to selection, but how broad a range of phenotypes it can produce remains unknown for many traits. Here we address this question using the mutually exclusive Rhodopsin 5 (Rh5) and Rhodopsin 6 (Rh6) expression pattern in Drosophila R8 photoreceptors, a neuronal differentiation readout that permits enumeration of a finite set of predicted qualitative phenotypic changes. Wild flies and wild-derived inbred lines from the Drosophila Genome Reference Panel 2 (DGRP2) showed extensive variation in Rh5/Rh6 expression, including shifts in the relative abundance of Rh5- and Rh6-expressing R8s, Rh5/Rh6 co-expression, and loss of Rh5 or Rh6. Among 205 DGRP2 lines, we observed examples spanning all eight predicted qualitative phenotype categories. We also identified causal coding and regulatory variants, including alleles of sevenless, Rh5 and Rh6, and an intronic deletion in melted. These results show that standing natural variation can span the full predicted range of qualitative phenotypes in this system.