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First published online May 1, 2006
Journal of Experimental Biology 209, 1944-1955 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02207

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Color discrimination in the red range with only one long-wavelength sensitive opsin

Guillermo Zaccardi^1,*, Almut Kelber¹, Marilou P. Sison-Mangus² and Adriana D. Briscoe²

¹ Vision Group, Department of Cell and Organism Biology, Lund University, Helgonavägen 3, S-22362 Lund, Sweden
² Comparative and Evolutionary Physiology Group, Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA

View larger version (32K): [in a new window]   Fig. 1. Arthropod opsin gene phylogeny. The phylogeny is based upon a neighbor-joining analysis of first and second nucleotide positions using the Tamura–Nei model of evolution with a correction for heterogeneous patterns of evolution among lineages. A total of 631 nucleotide sites were used. Numbers at the junctions indicate bootstrap replicates out of 1000 (given as a percentage) in which a particular node is supported. Red indicates cloned Heliconius erato opsin cDNAs. GenBank accession numbers for the sequences used in the reconstruction are as follows. Chelicerates: Limulus polyphemus (lateral eye, L03781; ocelli, L03782). Crustaceans: Procambarus clarkii (S53494). Insects: Anopheles gambiae [accession no. is given as supplementary information in Hill et al. (Hill et al., 2002)]; Antheraea pernyi (AB073299); Apis mellifera (UV, AF004169; Blue, AF004168; LW, U26026); Bombyx mori (LWRh1, AB064496), Camponotus abdominalis (LW, U32502; SW, AF042788); Cataglyphis bombycinus (LW, U32501; SW, AF042787); Danaus plexippus (UVRh, AY605546; BlueRh, AY605545; LWRh, AY605544); Drosophila melanogaster (Rh1, K02315; Rh2, M12896; Rh3, M17718; Rh4, M17730; Rh5, U67905; Rh6, Z86118); Homalodisca coagulata (AY588065); Manduca sexta (Manop1, L78080; Manop2, L78081; Manop3, AD001674); Megoura viciae (UV, AF189715; LW AF189714); Papilio glaucus (PglRh1, AF077189; PglRh2, AF077190; PglRh3, AF067080; PglRh5, AF077191; PglRh6, AF077192); Oncometopia nigricans (AY725781); Pieris rapae (PrL, AB177984); Schistocerca gregaria (Lo1, X80071; Lo2, X80072); Sphodromantis spp. (X71665). Full-length nucleotide sequences for the Bombyx mori UV, blue and L opsin coding regions were obtained using a tBlastx search of GenBank whole genome sequences (wgs), manually removing the introns in MacClade, and then comparing the coding sequences with partial B. mori opsin cDNAs reported in (Shimizu et al., 1998). The bar indicates the number of substitutions/site.

View larger version (28K): [in a new window]   Fig. 2. Spectral sensitivity of the photoreceptors calculated from the sensitivity maxima given in Struwe (Struwe, 1972) for H. erato (solid lines) and Briscoe et al. (Briscoe et al., 2003) for V. cardui (broken lines) using the template from Stavenga et al. (Stavenga et al., 1993). Peak sensitivity values for the short, medium and long wavelength visual pigments are identical between V. cardui and V. atalanta (not shown; G. Bernard, personal communication). Observe that both species have the medium wavelength photoreceptor peaking at 470 nm therefore the curves for both species coincide. The vertical dotted lines correspond to the wavelengths of the stimuli used.

View larger version (24K): [in a new window]   Fig. 3. Schematic views of the apparatus used to train and test the butterflies to the different colors. (A) Frontal view of the apparatus. (B) Lateral view of the apparatus. (C) The feeder disk.

View larger version (41K): [in a new window]   Fig. 4. Choice frequencies of H. erato and V. atalanta for the four colors after training, as a function of the ratio between the intensities of the rewarded color and the unrewarded color. The symbols represent the individual performance and the line the average. (A) Three V. atalanta trained to 620 nm as the rewarded color and 440 nm as unrewarded. All choices differ significantly from chance (P<0.05). (B) The same three butterflies as in A but this time 620 nm as the rewarded color and 590 as unrewarded. All choices differ significantly from chance (P<0.05). (C) Nine H. erato trained to 620 nm as the rewarded color and 590 nm as the unrewarded. The choices of every single animal differ significantly from chance (P<0.05). (D) The same nine animals from the previous experiment trained to 620 nm rewarded and 640 nm unrewarded. The choices of butterflies nos. 3, 4, 5 and 6 differ significantly from chance (P<0.05) at the intensity ratio 0.01.

View larger version (159K): [in a new window]   Fig. 5. In situ hybridizations of cryostat sections of the compound eye of H. erato using UVRh, BlueRh and LWRh digoxigenin-labeled antisense riboprobes. (A) UVRh and (B) BlueRh opsin mRNAs, respectively, detected using an alkaline phosphatase-conjugated anti-digoxigenin antibody. The insets show the magnification of the boxed region. Since the sections are consecutive, the position of the same ommatidium in A can be identified in B, as indicated by aligning the black circles. The butterflies express these two opsin mRNAs in three different ways in different ommatidia: S-S, S-M and M-M in the R1 and R2 photoreceptor cells. (C) Expression pattern of the LWRh opsin mRNA transcript. In every ommatidium in the main retina, six photoreceptor cells express the L opsin mRNA. (D) Close up view of the L opsin mRNA expression pattern in the R3-8 photoreceptor cells. Sections are at around 160 µm from the cornea. Scale bars, 50 µm (A–C); 20 µm (D).

View larger version (94K): [in a new window]   Fig. 6. Eye glow, pupillary pigments and lateral filtering pigments of H. erato (A–C) and V. atalanta (D–F) from the fronto-lateral eye region. (A) Eye glow of H. erato. Two classes of ommatidia can be observed, one of them reflects yellow and the other red. (B) Pupillary pigments at 190 µm from the cornea. (C) Lateral filtering pigments at 370 µm from the cornea vary between ommatidia (circles a and b) compared to the uniformly distributed pupillary pigments. (D) Eye glow of V. atalanta. Only one orange reflecting class exists. (E) Pupillary pigments at 180 µm from the cornea. (F). Pupillary pigments at 250 µm from the cornea. Uniform pupillary pigment density between ommatidia can be observed in all photoreceptor cells. Sections are 10 µm thick. Scale bars, 50 µm.