Reconstructing the ancestral butterfly eye: focus on the opsins

Abstract

SUMMARY The 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.

Spectral sensitivity of the principal eyes of sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae), larvae

“…Because the correlation between our experimental data and the template curves is very strong, the contribution of the -LW band to the sensitivity curve is likely to be relatively minor. Our measurements also demonstrate that the peak absorbency of the T. marmoratus opsin compares well with other insect UV photoreceptors, which typically have peak sensitivities at approximately 360nm (Briscoe, 2008;Stavenga and Arikawa, 2006;Tovee, 1995). A particularly close spectral similarity is observed to the Drosophila melanogaster Rh4 opsin, which absorbs maximally at 375nm (Feiler et al, 1992).…”

Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision

“…Unlike the phylogenetically conservative spectral positions of colour photoreceptors in hymenopteran trichromats [21,22], the spectral properties of different butterflies show a large degree of diversity [73 -75] and can be trichromatic, tetrachromatic or pentrachromatic [73,75]. Both molecular tuning of opsin genes [73,76] and pigment filtering [77] suggest that butterfly spectral sensitivity differences evolved relatively rapidly, leading to a large degree of diversity of colour capabilities in these insects [73]. It is thus unlikely that butterfly pollinators, when considered as a group, could explain the fit of data in figure 2, because the colour discrimination capabilities of these insects would, in some cases, predict very different flower colours.…”

Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor

“…Aquatic taxa including teleost fish (Carleton and Kocher, 2001;Bowmaker and Hunt, 2006) and stomatopods (Cronin and Marshall, 1989;Porter et al, 2009) do have substantial spectral diversity of photoreceptors between related species, which can often be related to the spectral variation in ambient illumination in water. Among terrestrial animals, dragonflies (Futahashi et al, 2015) and butterflies (Briscoe, 2008) are known for the diversity of their photoreceptor spectral sensitivities, but the evolutionary causes and physiological significance of these differences remain unclear, and there is limited evidence for sexual dimorphism in photoreceptor spectral sensitivities (but see below).…”

“…The butterfly eye ground plan seems to have retained the ancestral form with three opsin-based photoreceptors, UV, B and LW, having wavelengths of maximum sensitivity at about 360, 470 and 560 nm, respectively (Briscoe and Chittka, 2001;Briscoe, 2008). Butterfly ommatidia contain nine photoreceptor cells R1-R9, whose photosensitive membranes form a fused rhabdom ( Fig.…”