Sex-limited diversification of the eye in Heliconius cydno butterflies.

Abstract

Butterflies have evolved a remarkable diversity in eye organization to support a range of vision-based behaviors including courtship, oviposition, and foraging. This diversity has been surveyed extensively across the butterfly phylogeny, but variation across closely related species remains less clear. We compared eye organization in Heliconius cydno, a clade of mimetic, Neotropical butterflies that have been studied in the context of wing coloration and courtship. Using a combination of eyeshine and opsin immunohistochemistry, we identified several sexually dimorphic features of eye organization where male eyes varied with species and female eyes did not. These features included the distribution of a red screening pigment across the eye, co-expression of the two UV opsins within single photoreceptors, and the relative distribution of UV and blue opsin expression in R1/R2 photoreceptors. Together, this suggests a shift in H. cydno males from an ancestor strongly biased towards the expanded Nymphalid mosaic characterized by blue and long wavelength opsin co-expression, red screening pigment, and green vs. red inter-photoreceptor opponency to one biased towards the basic mosaic consisting of UV-UV, Blue-Blue, and UV-Blue ommatidia. We hypothesize that this sex-limited variability may function to adapt these butterflies to sexually dimorphic behaviors like courtship and oviposition in the context of the natural light environment.