True UV color vision in a butterfly with two UV opsins

Abstract

True 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.

Multiple mechanisms of photoreceptor spectral tuning following loss of UV color vision inHeliconiusbutterflies

“…Meanwhile in melpomene/cydno species, expression of full-length UVRh2 is low but not absent, even though protein expression is missing from the eye. Consistent with a loss of the UV2 R1 and R2 cell, our behavioral experiments indicate that both male and female H. melpomene are unable to discriminate between 380 nm and 390 nm light (Finkbeiner and Briscoe, 2020). Thus, it seems likely that the silvaniforms downregulated UVRh2 expression earlier than H. melpomene did.…”

“…This suggests a loss in these two species of the 390 nm cell type found in H. erato . Behavioral tests of H. melpomene confirm adult males and females are unable to discriminate 380 nm from 390 nm light (Finkbeiner and Briscoe, 2020). Intracellular recordings reported here reveal a single UV sensitive R1 and R2 photoreceptor cell type in both H. melpomene and H. ismenius , with peak sensitivity or λ max = 365 nm (Figure 1D), consistent with behavioral experiments.…”

“…Butterflies in the genus Heliconius have superb color vision from short UV to near-infrared wavelengths (Finkbeiner et al, 2017; Finkbeiner and Briscoe, 2020; McCulloch et al, 2016a; Zaccardi et al, 2006). The morphological basis of Heliconius color vision is the compound eye, which is similar in structure to other butterflies.…”

“…In the sexually dimorphic visual system of Heliconius erato , females express UVRh1 and UVRh2 opsins while males only express UVRh2 (Figure 1B). Intracellular recordings and behavioral experiments showed that H. erato females have two physiologically distinct UV photoreceptor cell types, and that these conferred true UV color vision in females only (Finkbeiner and Briscoe, 2020; McCulloch et al, 2016a). Differences in the retinal mosaics across species and sexes showcase Heliconius as an evolutionary model to study incipient visual system divergence (McCulloch et al, 2017).…”

“…Thus, it seems likely that the silvaniforms downregulated UVRh2 expression earlier than H. melpomene did. Our previous work suggested that the Heliconius visual system (as exemplified by H. erato ), likely compensated after neofunctionalization of UVRh2 via spectral tuning to accommodate a new color channel (Finkbeiner and Briscoe, 2020; McCulloch et al, 2016a). As divergence went on, how did the subsequent loss of this same receptor in some lineages affect spectral tuning of their remaining photoreceptors?…”