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First published online May 19, 2008
Journal of Experimental Biology 211, 1805-1813 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013045
The adaptive evolution and processing of sensory systems |
Reconstructing the ancestral butterfly eye: focus on the opsins
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
e-mail: abriscoe{at}uci.edu
Accepted 26 November 2007
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, 
max, 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.
Key words: eye evolution, color vision, photoreceptor, rhodopsin, visual pigment, opsin, sexual dimorphism
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