Color discrimination in the red range with only one long-wavelength sensitive opsin

Abstract

SUMMARY The basic precondition for color vision is the presence of at least two receptor types with different spectral sensitivities. The sensitivity of a receptor is mostly defined by the opsin-based visual pigment expressed in it. We show here, through behavioral experiments, that the nymphalid butterfly Heliconius erato, although it expresses short and medium wavelength opsins and only one long wavelength opsin, discriminates colors in the long-wavelength range (590 nm, 620 nm and 640 nm), whereas another nymphalid, Vanessa atalanta, despite having color vision, is unable to do so. In the eyes of H. erato we identified filtering pigments very close to the rhabdom which differ between ommatidia and produce the yellow and red ommatidial reflection seen under orthodromic illumination. The eyes of V. atalanta lack the filtering pigments, and reflect a homogeneous orange. We hypothesize that the filtering pigments found in the eyes of H. erato may shift the spectral sensitivity peak of the long wavelength receptors in some ommatidia towards longer wavelengths. The comparison of the signals between the two new receptor types makes color discrimination in the red range possible. To our knowledge, this is the first behavioral proof of color vision based on receptors expressing the same opsin.

Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes

“…These data suggest that a sexually dimorphic eye may represent the ancestral state in insects. However, other more basal butterflies that have been examined, such as the swallowtail, the painted lady, the heliconian and the monarch butterfly, do not have sexually dimorphic patterns of opsin mRNA expression (Kitamoto et al, 1998;Briscoe et al, 2003;Sauman et al, 2005;Zaccardi et al, 2006). Rather, our data suggest that sexually dimorphic male eyes, expressing predominantly UV and B opsins, may have evolved independently in insects.…”

“…It is therefore possible that L. rubidus has pentachromatic vision in ventral retina based primarily on four opsins and this pink non-opsin pigment. Filtering pigments of similar effect have been observed for the LW receptors of Papilio xuthus and Pieris rapae (Arikawa et al, 1999;Wakakuwa et al, 2004), and have been shown to be important for butterfly color vision (Zaccardi et al, 2006).…”

“…The presence of a fourth visual pigment mRNA BRh2, together with UVRh and BRh1, furnishes Lycaena with six ommatidial subtypes in the ventral eye area (Fig.·4), twice the number found in any other lepidopteran (Arikawa, 2003;Briscoe et al, 2003;White et al, 2003;Sauman et al, 2005;Zaccardi et al, 2006). Even in Pieris rapae (Arikawa et al, 2005), which as noted above has independently evolved a violet receptor from a duplicate blue opsin gene, only three ommatidial types have been reported: those expressing UV-UV, UV-B, and V-V opsin mRNAs.…”

“…To explain the four major evolutionary innovations we have identified in L. rubidus eye (duplicate blue opsin cDNAs, novel R1 and R2 photoreceptor subtypes, co-expression of B and LW opsins and male-only BRh1 opsin expression in R3-8 cells) we M. P. Sison-Mangus and others propose the following evolutionary scheme (Fig.·6): Nymphalids, the closest outgroup for which gene expression data are available, have three kinds of ommatidia: UV and B opsin mRNAs are expressed in R1 and R2 photoreceptor cells in a non-overlapping fashion, and the LW opsin mRNA is expressed in the R3-8 photoreceptor cells (Briscoe et al, 2003;Sauman et al, 2005;Zaccardi et al, 2006). This pattern is also found in the moth Manduca sexta , and likely represents the ancestral lepidopteran eye plan.…”

“…Lycaenids in particular comprise the second largest of the butterfly families, with more than 4000 species named worldwide, many of which are found in South America (Johnson and Coates, 1999). With a mounting abundance of physiological (Eguchi et al, 1982;Kinoshita et al, 1997), molecular (see below) and behavioral data (Zaccardi et al, 2006) pointing to phenotypically variable butterfly visual systems, it seems increasingly important to consider the Although previous investigations have shown that wing coloration is an important component of social signaling in butterflies, the contribution of opsin evolution to sexual wing color dichromatism and interspecific divergence remains largely unexplored. Here we report that the butterfly Lycaena rubidus has evolved sexually dimorphic eyes due to changes in the regulation of opsin expression patterns to match the contrasting life histories of males and females.…”