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First published online August 3, 2006
Journal of Experimental Biology 209, 3079-3090 (2006)
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
1 Comparative and Evolutionary Physiology Group, Department of Ecology and
Evolutionary Biology, 321 Steinhaus Hall, University of California, Irvine, CA
92697, USA
2 Department of Electrical Engineering, University of Washington, Seattle,
WA 98195-2500, USA
3 Functional Morphology Group, Department of Developmental Biology,
University of Erlangen-Nuremberg, 91058 Erlangen, Germany
* Author for correspondence (e-mail: abriscoe{at}uci.edu)
Accepted 5 June 2006
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. The L. rubidus eye contains four
visual pigments with peak sensitivities in the ultraviolet (UV;
max=360 nm), blue (B; max=437 nm and 500
nm, respectively) and long (LW; max=568 nm) wavelength
range. By combining in situ hybridization of cloned opsinencoding
cDNAs with epi-microspectrophotometry, we found that all four opsin mRNAs and
visual pigments are expressed in the eyes in a sex-specific manner. The male
dorsal eye, which contains only UV and B (max=437 nm)
visual pigments, indeed expresses two short wavelength opsin mRNAs,
UVRh and BRh1. The female dorsal eye, which also has the UV
and B (max=437 nm) visual pigments, also contains the LW
visual pigment, and likewise expresses UVRh, BRh1 and
LWRh mRNAs. Unexpectedly, in the female dorsal eye, we also found
BRh1 co-expressed with LWRh in the R3-8 photoreceptor cells.
The ventral eye of both sexes, on the other hand, contains all four visual
pigments and expresses all four opsin mRNAs in a non-overlapping fashion.
Surprisingly, we found that the 500 nm visual pigment is encoded by a
duplicate blue opsin gene, BRh2. Further, using molecular
phylogenetic methods we trace this novel blue opsin gene to a duplication
event at the base of the Polyommatine+Thecline+Lycaenine radiation. The blue
opsin gene duplication may help explain the blueness of blue lycaenid
butterflies.
Key words: eye evolution, sexual selection, visual pigment, color vision, butterfly, Lycaena rubidus
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