Sex-limited diversification of the eye in Heliconius butterflies

Abstract

Butterflies have evolved an immense 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, and here we take a complementary approach to characterize the eye within a group of closely related Heliconius butterflies. Using a combination of immunostaining for different opsins and eyeshine for determining the distribution of light-filtering screening pigments, we identified several sexually dimorphic features of eye organization where male eyes varied and female eyes did not. Ultraviolet (UV) sensitive photoreceptors varied in which of two UV opsins were expressed, including co-expression of both within single photoreceptors, and these differences were consistent with a role in courtship and conspecific identification. Additional differences across species and sex included the distribution of three ommatidial types defined by the expression pattern of UV and blue opsins, the distribution of a red screening pigment, and which ommatidial types expressed the red screening pigment. We hypothesize that female eyes are optimized for a dimorphic behavior such as oviposition, while male eyes adapt to other selective pressures such as the local light environment.