Sexual Dimorphism of Short-Wavelength Photoreceptors in the Small White Butterfly,Pieris rapae crucivora

Abstract

The eyes of the female small white butterfly, Pieris rapae crucivora, are furnished with three classes of short-wavelength photoreceptors, with sensitivity peaks in the ultraviolet (UV) ( max ϭ 360 nm), violet (V) ( max ϭ 425 nm), and blue (B) ( max ϭ 453 nm) wavelength range. Analyzing the spectral origin of the photoreceptors, we isolated three novel mRNAs encoding opsins corresponding to shortwavelength-absorbing visual pigments. We localized the opsin mRNAs in the retinal tissue and found that each of the short-wavelengthsensitive photoreceptor classes exclusively expresses one of the opsin mRNAs. We, accordingly, termed the visual pigments PrUV, PrV, and PrB, respectively. The eyes of the male small white butterfly also use three classes of short-wavelength photoreceptors that equally uniquely express PrUV, PrV, and PrB. However, whereas the spectral sensitivities of the male photoreceptors with PrUV and PrB closely correspond to those of the female, the male photoreceptor expressing PrV has a double-peaked blue (dB) spectral sensitivity, strongly deviating from the spectral sensitivity of the female V photoreceptor. The male eyes contain a pigment that distinctly fluoresces under blue-violet as well as UV excitation light. It coexists with the dB photoreceptors and presumably acts as a spectral filter with an absorbance spectrum peaking at 416 nm. The narrow-band spectral sensitivity of the male dB photoreceptors probably evolved to improve the discrimination of the different wing colors of male and female P. rapae crucivora in the short-wavelength region of the spectrum.

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

“…To our knowledge, no other insects besides pierid and lycaenid butterflies have two blue opsin genes. Our finding of independent duplication events is quite consistent with the very different max values (425·nm and 453·nm) of the pierid blue visual pigments (Arikawa et al, 2005) compared to the lycaenid ( max =437·nm and 500·nm, respectively). Our results also indicate (bootstrap support=100%) that the L. rubidus blue opsin gene duplication event occurred before the radiation of the coppers, hairstreaks and blues.…”

“…In the case of the small white cabbage butterfly, Pieris rapae (Pieridae) (Arikawa et al, 2005), three short wavelength receptors were found, sensitive to ultraviolet ( max =360·nm), violet ( max =425·nm) and blue ( max =453·nm) light, and each expressing a unique opsin. A spectral filtering pigment was found co-expressed with the blue opsin only in males, producing a uniquely narrow blue receptor, highlighting the changes in the spatial expression patterns of non-opsin filtering pigments as a mechanism for producing a sexually dimorphic retina.…”

“…The situation in L. rubidus differs markedly from that of the nymphalid butterflies Vanessa cardui or the monarch Danaus plexippus, in which only three opsin mRNAs are expressed (UV, B, and LW) in the photoreceptor cells of the adult eye (Briscoe et al, 2003;Sauman et al, 2005), or that of the swallowtail butterfly, in which three duplicate LW opsin genes are expressed (Briscoe, 1998;Kitamoto et al, 1998). The L. rubidus opsin expression pattern does, however, resemble the situation in Pieris rapae, in which duplicate B opsin genes are also expressed in the eye (Arikawa et al, 2005) (but see below).…”

“…Within the true butterflies (Papilionoidea) the current understanding of familial relationships is (Papilionidae+(Pieridae+(Nymphalidae+(Riodinidae+Lycaeni dae)))) (Wahlberg et al, 2005), where papilionid and pierid butterflies represent the most basal lineages, and riodinid and lycaenid the most derived. Because the two pairs of B opsin genes identified from pierid (Pieris rapae) (Arikawa et al, 2005) and lycaenid butterflies (this study) are from distantly related families, we were interested in testing the hypothesis that the blue opsin genes of pierids and lycaenids evolved independently. We therefore screened eye-specific cDNA libraries from an additional ten butterfly taxa from four families (supplementary material Table·S3).…”

“…In the sphingid moth, the painted lady and monarch butterfly, these visual pigments are encoded by paralogous UV, B and LW opsin genes, which were present in the ancestor of all lepidopterans (Briscoe et al, 2003;White et al, 2003;Sauman et al, 2005). Deviations from this basic plan have been described in the most primitive of butterfly families, the papilionids, in which two rounds of duplication of the LW eye opsin gene have occurred (Briscoe, 1998;Kitamoto et al, 1998;Briscoe, 2001); and in the pierids, in which a duplicate blue opsin gene has been reported (Arikawa et al, 2005). In all butterfly species studied, opsin mRNA expression in the eye is similar between the sexes: the R1 and R2 photoreceptor cells express either UV or B opsin mRNAs and the R3-9 photoreceptors express LW opsin mRNAs.…”