Abstract

Butterflies use color vision extensively to navigate the natural world. Their retinas are more complex than those found in Drosophila, where development and patterning has been heavily studied. Instead of the eight photoreceptors found in flies, butterflies have an additional ninth photoreceptor per ommatidium (“unit eye”). They also have three main types of ommatidia instead of the two distributed stochastically in the fly retina. We set out to determine how butterflies generate increased sensory receptor diversity to provide an expanded range of color vision, and how much of the retinal patterning network from Drosophila they reuse. We show that the regulatory network that defines photoreceptor subtypes in Drosophila is redeployed in butterflies (Papilio xuthus and Vanessa cardui) to generate additional subtypes. The R7 photoreceptor marker Prospero is expressed in two rather than one photoreceptors per ommatidium. In Drosophila, a stochastic decision to express the transcription factor Spineless in R7 determines which of two subtypes of ommatidia is specified. CRISPR knock-out of Spineless in butterflies shows that Spineless also controls stochastic choice in each of the two R7s, suggesting a deep evolutionary conservation of stochastic patterning mechanisms. Having two stochastically distributed types of R7s allows for specification of three ommatidial types instead of two, which in turn allowed for the evolution and deployment of additional opsins, tetrachromacy, and improved color vision. These efforts provide evidence that our extensive knowledge of patterning in the Drosophila visual system applies to other groups, and that adaptation for specific visual requirements can occur through modification of this network.