3079
The Journal of Experimental Biology 209, 3079-3090 Published by The Company of Biologists 2006 doi:10.1242/jeb.02360
Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes Marilou P. Sison-Mangus1, Gary D. Bernard2, Jochen Lampel3 and Adriana D. Briscoe1,* 1Comparative and Evolutionary Physiology Group, Department of Ecology and Evolutionary Biology, 321 Steinhaus Hall, University of California, Irvine, CA 92697, USA, 2Department of Electrical Engineering, University of Washington, Seattle, WA 98195-2500, USA and 3Functional Morphology Group, Department of Developmental Biology, University of Erlangen-Nuremberg, 91058 Erlangen, Germany *Author for correspondence (e-mail: [email protected])
Accepted 5 June 2006
Summary Although previous investigations have shown that wing pigments, also contains the LW visual pigment, and coloration is an important component of social signaling in likewise expresses UVRh, BRh1 and LWRh mRNAs. butterflies, the contribution of opsin evolution to sexual Unexpectedly, in the female dorsal eye, we also found wing color dichromatism and interspecific divergence BRh1 co-expressed with LWRh in the R3-8 photoreceptor remains largely unexplored. Here we report that the cells. The ventral eye of both sexes, on the other hand, butterfly Lycaena rubidus has evolved sexually dimorphic contains all four visual pigments and expresses all four eyes due to changes in the regulation of opsin expression opsin mRNAs in a non-overlapping fashion. Surprisingly, patterns to match the contrasting life histories of males we found that the 500·nm visual pigment is encoded by a and females. The L. rubidus eye contains four visual duplicate blue opsin gene, BRh2. Further, using molecular pigments with peak sensitivities in the ultraviolet (UV; phylogenetic methods we trace this novel blue opsin max=360·nm), blue (B; max=437·nm and 500·nm, gene to a duplication event at the base of the respectively) and long (LW; max=568·nm) wavelength Polyommatine+Thecline+Lycaenine radiation. The blue range. By combining in situ hybridization of cloned opsin- opsin gene duplication may help explain the blueness of encoding cDNAs with epi-microspectrophotometry, we blue lycaenid butterflies. found that all four opsin mRNAs and visual pigments are expressed in the eyes in a sex-specific manner. The male Supplementary material available online at dorsal eye, which contains only UV and B (max=437·nm) http://jeb.biologists.org/cgi/content/full/209/16/3079/DC1 visual pigments, indeed expresses two short wavelength opsin mRNAs, UVRh and BRh1. The female dorsal eye, Key words: eye evolution, sexual selection, visual pigment, color which also has the UV and B (max=437·nm) visual vision, butterfly, Lycaena rubidus.
Introduction mediated components of courtship have typically been put Ever since Darwin’s time (Darwin, 1874), there has been forth in the absence of information about sensory receptors. intense interest in understanding the origins and evolution of Previous studies of both butterfly wing color cues and color sexually dimorphic traits. Butterflies offer spectacular vision have focused on papilionid, pierid or nymphalid families examples of sexual dimorphism associated with wing color (Kelber et al., 2003). Little attention, however, has been paid variation between males and females (sexual dichromatism). to the youngest of butterfly families, the riodinids or the The use of wing color cues in speciation (Silberglied, 1979) lycaenids, because they tend to be small and hard to distinguish and sexual selection (Obara, 1970) has long been recognized. to the human eye. Lycaenids in particular comprise the second Sympatric butterfly relatives that look similar from the human largest of the butterfly families, with more than 4000 species perspective are readily distinguished, for instance, by UV- named worldwide, many of which are found in South America based signals (Silberglied, 1979). Moreover, females have (Johnson and Coates, 1999). With a mounting abundance of been shown to use species-specific UV reflectance patterns to physiological (Eguchi et al., 1982; Kinoshita et al., 1997), identify mates (Silberglied and Taylor, 1973; Rutowski, 1977; molecular (see below) and behavioral data (Zaccardi et al., Robertson and Monteiro, 2005). Nonetheless, discussions of 2006) pointing to phenotypically variable butterfly visual the evolution of butterfly wing colors in relation to visually systems, it seems increasingly important to consider the
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