UC Irvine

Gene duplications sometimes result in large evolutionary shifts in adaptation, but often no phenotypic change occurs after duplication. In animals, molecular genetic changes, including duplications in opsin genes have resulted in highly diverse visual phenotypes. Unlike the diversity of vision-related phenotypes among orders and families, visual systems are mostly conserved among closely related species, and evidence is limited as to how visual traits initially diverge. The neotropical butterfly genus, Heliconius, is a good system for addressing these questions. Heliconius has duplicated UV opsin genes (UVRh1 and UVRh2) coincident with a UV-yellow wing pigment, a known sexual visual cue. I hypothesized that the Heliconius-specific opsin duplication has led to photoreceptor neofunctionalization in the genus, which might affect visual system evolution and divergence in the genus due to the importance of UV signals in Heliconius.

To understand the phenotypic effects of UV gene duplication in H. erato, I developed an intracellular recording technique in the lab that measures photoreceptor spectral sensitivities. I also compared differences in opsin expression and retinal mosaics across 23 species in the genus, using immunohistochemistry and RNA-Sequencing. Combining this data in a phylogenetic context, I analyzed the evolutionary history of the opsins and their expression patterns in Heliconius. Intracellular recordings confirm two distinct female-specific UV-sensitive cells in H. erato females, but males lack the UVRh1 cell. Unlike other groups with conserved eye design among closely-related species, I discovered a high diversity of both sex- and clade-specific retinal mosaics within the genus. I found three unique forms of sexual dimorphism, multiple independent pseudogenizations of UVRh2, and the independent evolution of a retinal mosaic in separate clades. The proportions of ommatidial types are tightly regulated within each species and sex. These patterns indicate that Heliconius species with only one UV cell subtype have higher proportions of blue cells, perhaps as a secondary method for detecting the genus-specific UV-yellow wing pigment.

The spectacular diversity in opsin expression represents the rarely-seen incipient stages of visual system divergence. Novel UV photoreceptor subtypes evolved in Heliconius via opsin gene duplication, and subsequent varying selection pressures have likely caused the increased diversity of retinal mosaics in Heliconius.