Reconstructing the ancestral butterfly eye: focus on the opsins

Abstract

SUMMARYThe eyes of butterflies are remarkable, because they are nearly as diverse as the colors of wings. Much of eye diversity can be traced to alterations in the number, spectral properties and spatial distribution of the visual pigments. Visual pigments are light-sensitive molecules composed of an opsin protein and a chromophore. Most butterflies have eyes that contain visual pigments with a wavelength of peak absorbance, λmax, in the ultraviolet (UV, 300–400 nm), blue (B, 400–500 nm) and long wavelength (LW, 500–600 nm) part of the visible light spectrum,respectively, encoded by distinct UV, B and LW opsin genes. In the compound eye of butterflies, each individual ommatidium is composed of nine photoreceptor cells (R1–9) that generally express only one opsin mRNA per cell, although in some butterfly eyes there are ommatidial subtypes in which two opsins are co-expressed in the same photoreceptor cell. Based on a phylogenetic analysis of opsin cDNAs from the five butterfly families,Papilionidae, Pieridae, Nymphalidae, Lycaenidae and Riodinidae, and comparative analysis of opsin gene expression patterns from four of the five families, I propose a model for the patterning of the ancestral butterfly eye that is most closely aligned with the nymphalid eye. The R1 and R2 cells of the main retina expressed UV–UV-, UV–B- or B–B-absorbing visual pigments while the R3–9 cells expressed a LW-absorbing visual pigment. Visual systems of existing butterflies then underwent an adaptive expansion based on lineage-specific B and LW opsin gene multiplications and on alterations in the spatial expression of opsins within the eye. Understanding the molecular sophistication of butterfly eye complexity is a challenge that,if met, has broad biological implications.