True UV color vision in a butterfly with two UV opsins

Abstract

ABSTRACTTrue color vision in animals is achieved when wavelength discrimination occurs based on chromatic content of the stimuli, regardless of intensity. In order to successfully discriminate between multiple wavelengths, animals must use at least two photoreceptor types with different spectral sensitivity peaks.Heliconius butterflies have duplicate UV opsin genes, which encode two kinds of photoreceptors with peak sensitivities in the ultraviolet and violet, respectively. In H. erato, the ultraviolet photoreceptor is only expressed in females.Evidence from intracellular recordings suggests female H. erato may be able to discriminate between UV wavelengths, however, this has yet to be tested experimentally.Using an arena with a controlled light setting, we tested the ability of H. erato, and two species lacking the violet receptor, H. melpomene and outgroup Eueides isabella, to discriminate between two ultraviolet wavelengths, 380 and 390 nm, as well as two blue wavelengths, 400 and 436 nm, after being trained to associate each stimulus with a food reward. Wavelength stimuli were presented in varying intensities to rule out brightness as a cue.We found that H. erato females were the only butterflies capable of color vision in the UV range; the other butterflies had an intensity-dependent preference for UV stimuli. Across species, both sexes showed color vision in the blue-range.Models of H. erato color vision suggest that females have an advantage over males in discriminating the inner UV-yellow corolla of Psiguria pollen flowers from the surrounding outer orange petals, while previous models (McCulloch et al. 2017) suggested that H. erato males have an advantage over females in discriminating Heliconius 3-hyroxykynurenine (3-OHK) yellow wing coloration from non-3-OHK yellow wing coloration found in mimics.These results provide some of the first behavioral evidence for UV color discrimination in Heliconius females in the context of foraging, lending support to the hypothesis (Briscoe et al. 2010) that the duplicated UV opsin genes function together in UV color vision. Taken together, the sexually dimorphic visual system of H. erato appears to have been shaped by both sexual selection and sex-specific natural selection.