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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
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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,*

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


Figure 1
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  		Fig. 1. Anatomical overview of an L. rubidus ommatidium and non-opsin pigment expression. (A) Diagram of a typical ommatidium. Longitudinal (left) and transverse (right) view of an ommatidium located in the ventral domain of the eye. Purple pupillary pigments are present in R1-8 photoreceptor cells regulating the amount of light entering the ommatidium. (B) The dorsal eye lacks the pink filtering pigment. Transverse unstained Epon sections were examined by DIC microscopy. Arrows denote rhabdoms (rh). (C) In the ventral eye, most ommatidia contain a pink filtering pigment (arrowheads), which is lacking in other ommatidia (arrow). Basement membrane (bm), cornea (c), rhabdom (rh), tapetum (tp), crystalline cones (cc). Scale bars, 5 µm (A), 10 µm (B).

 

Figure 2
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  		Fig. 2. Sex differences (A,C,E,G, males; B,D,F,H, females) in wing color pattern, eyeshine, eye reflectance spectra and visual pigment absorbance spectra. (A,B) (A) UV-reflecting scales (iridescent purple) on the lower forewing and outer hindwing margins of males, (B) Non-UV-reflecting scales on wings of females. Reflectance spectra of both male and female dorsal wings are shown elsewhere (Bernard and Remington, 1991Go). (C,D) Eyeshine from the dorsal eye of (C) a male and (D) a female showing strongly sexually dimorphic coloration. (E,F) Analysis of experimental reflectance spectra (black dots) from dorsal eye ommatidia of (E) males and (F) females, based on a computational model of pigment content; spectrum was obtained after having stripped the visual pigment with {lambda}max=568 nm (P568) (red circles, female only); metarhodopsin 495 nm (orange squares); 437 nm (green diamonds), retinoid-binding protein 395 nm (dark blue diamonds); and 360 nm (light blue diamonds). (G,H) Absorbance spectra for the visual pigments estimated from epimicrospectrophotometry in the dorsal eyes of males (E, {lambda}max=437 nm and 360 nm) and females (F, {lambda}max=568 nm, 437 nm and 360 nm).

 

Figure 3
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  		Fig. 3. Sexually dimorphic opsin expression (A,C,E,G, males; B,D,F,H, females). LWRh expression in male eye (A) and female eye (B). Inset in B shows expression in R3-8. BRh1 expression in male (C) and female (D). Inset in D shows expression in R3-8. UVRh expression in male (E) and female (F). BRh2 expression in male (G) and female (H). Tangential sections are shown for each panel. Scale bars, 100 µm.

 

Figure 4
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  		Fig. 4. Non-overlapping UVRh, BRh1 and BRh2 expression in R1 and R2 photoreceptor cells. (A-C) Ventral views. (A) Tangential section showing UVRh expression in R1 and R2 photoreceptor cells in the ventral retina. (B) Section adjacent to A showing BRh1 mRNA expression in R1 and R2 cells in the ventral retina that was non-overlapping with UVRh expression. Broken circles in each panel indicate identical ommatidia in adjacent sections. (C) Section adjacent to B showing BRh2 expression in R1 and R2 cells in the ventral retina that was non-overlapping with UVRh and BRh1 mRNA expression. Five different types of ommatidia are depicted in each panel: UVRh-UVRh (one arrowhead), UVRh-BRh1 (short arrow); UVRh-BRh2 (double short arrows); BRh1-BRh1 (long arrow); BRh1-BRh2 (double arrowheads). A sixth combination BRh2-BRh2 was also observed (data not shown). (D-F) Dorsal views. (D) Tangential section showing UVRh expression in nearly all R1 and R2 cells in the dorsal retina. (E) Tangential section showing BRh1 expression in a small number of R1 and R2 (and all R3-R8) cells in the dorsal retina. Inset (big square) shows BRh1 expressed in R1, as well as R3-8 cells; small square shows BRh1 expressed in R1-R8 cells. (F) Section adjacent to D showing no BRh2 mRNA expression in dorsal retina. Broken circles indicate identical ommatidia in adjacent sections. Three different types of ommatidia were found: UVRh-UVRh (arrowhead), UVRh-BRh1 (short arrow), BRh1-BRh1 (long arrow).

 

Figure 5
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  		Fig. 5. Phylogeny of lepidopteran blue opsin genes. The tree is based upon a neighbor-joining (NJ) analysis of 1077 nucleotide sites, using Tamura-Nei distance and heterogeneous pattern of nucleotide substitution among lineages. Bootstrap values shown are based upon 500 maximum likelihood (ML) bootstrap replicates determined using the GTR+{Gamma}+I model with estimated gamma shape parameter=0.574 and proportion of invariant sites=0.1474. GenBank accession numbers for sequences are provided in supplementary material Table S3. Inset: Dorsal wing of a male Polyommatus icarus, one of the lycaenids surveyed.

 

Figure 6
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  		Fig. 6. Evolutionary steps leading to the adaptive evolution of the blue opsin duplication and the evolution of sexually dimorphic eyes. Step (1). Duplication of the blue opsin gene. Step (2) Neofunctionalization of the B2 opsin (BRh2) to an extremely red-shifted (500 nm) peak absorbance. Step (3) Subfunctionalization of the BRh2 expression to a subset of the R1 and R2 photoreceptor cells that are non-overlapping with BRh1 and UVRh. Step (4) Alteration in the regulation of BRh1 (B1) spatial expression to include co-expression with LWRh (LW) the outer R3-8 photoreceptor cells of dorsal eye of both sexes. Step (5) Suppression of LWRh opsin expression in dorsal eye of males only. Color code: black, UV opsin; dark blue, B1 opsin; light blue, B2 opsin; orange, LW opsin.

 




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