Evolution of the Compound Eye and Visual Preference in Butterflies

The evolution of visual systems is tightly linked to the diversification of visually guided behaviors, shaped by complex ecological pressures such as adaptation to varied diel niches and mate choice. This dissertation first synthesizes the remarkable cellular innovations and diversity within the lepidopteran compound eye. I review eye evolution across anatomical and molecular scales, highlighting how opsins and filtering pigments generate diverse spectral sensitivities across butterflies and moths. These diverse photoreceptors are arranged in complex retinal mosaics governed by largely unknown regulatory mechanisms. To investigate the genetic and regulatory mechanisms driving eye cell type evolution, I characterized compound eye evolution across Heliconius butterflies, which are renowned for diverse wing color patterns and complex visually guided behaviors. Within a single population polymorphic for mate preference, I integrated 3D chromatin architecture, single-cell transcriptomics, and epigenomics to map cell-type-specific transcriptomic divergence linked to male mate choice. This multi-modal approach identified sens-2 as a key preference gene expressed in glia. Extending this work across a speciation continuum to reproductively isolated species, I utilized comparative single-cell transcriptomics to demonstrate that visual system evolution is shaped not only by transcriptomic divergence but also by rapid shifts in cellular composition. Furthermore, this cross-species comparison revealed that photoreceptors, particularly the color-sensing R7, exhibit significantly accelerated rates of gene expression evolution compared to downstream neurons and glia. By characterizing novel R7 photoreceptor subtypes, I showed that cellular subfunctionalization can arise through the co-option of existing gene regulatory networks. Together, this dissertation provides a comprehensive view of compound eye evolution and the mechanisms by which novel cell types evolve.