Not all butterfly eyes are created equal: Rhodopsin absorption spectra, molecular identification, and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui

Adriana D. Briscoe, Gary D. Bernard, Allan S. Szeto, Lisa M Nagy, Richard H. White

Research output: Contribution to journalArticle

77 Citations (Scopus)

Abstract

Surveys of spectral sensitivities, visual pigment spectra, and opsin gene sequences have indicated that all butterfly eyes contain ultraviolet-, blue-, and green-sensitive rhodopsins. Some species also contain a fourth or fifth type, related in amino acid sequence to green-sensitive insect rhodopsins, but red shifted in absorbance. By combining electron microscopy, epimicrospectrophotometry, and polymerase chain reaction cloning, we found that the compound eye of Vanessa cardui has the typical ultrastructural features of the butterfly retina but contains only the three common insect rhodopsins. We estimated lambda-max values and relative densities of the rhodopsins in the Vanessa retina (0.72, P530; 0.12, P470; and 0.15, P360) from microspectrophotometric measurements and calculations based on a computational model of reflectance spectra. We isolated three opsin-encoding cDNA fragments that were identified with P530, P470, and P360 by homology to the well-characterized insect rhodopsin families. The retinal mosaic was mapped by opsin mRNA in situ hybridization and found to contain three kinds of ommatidia with respect to their patterns of short wavelength rhodopsin expression. In some ommatidia, P360 or P470 was expressed in R1 and R2 opposed receptor cells; in others, one cell expressed P360, whereas its complement expressed P470. P530 was expressed in the other seven cells of all ommatidia. P470-expressing cells were abundant in the ventral retina but nearly absent dorsally. Our results indicated that there are major differences between the color vision systems of nymphalid and papilionid butterflies: the nymphalid Vanessa has a simpler, trichromatic, system than do the tetrachromatic papilionids that have been studied.

Original languageEnglish (US)
Pages (from-to)334-349
Number of pages16
JournalJournal of Comparative Neurology
Volume458
Issue number4
DOIs
StatePublished - Apr 14 2003

Fingerprint

Carduus
Butterflies
Rhodopsin
Retina
Opsins
Messenger RNA
Insects
Color Vision
Specific Gravity
Retinal Pigments
In Situ Hybridization
Organism Cloning
Amino Acid Sequence
Electron Microscopy
Complementary DNA
Polymerase Chain Reaction

Keywords

  • Color vision
  • Lepidoptera
  • Nymphalidae
  • Photoreceptor
  • Visual pigment

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Not all butterfly eyes are created equal: Rhodopsin absorption spectra, molecular identification, and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui",
abstract = "Surveys of spectral sensitivities, visual pigment spectra, and opsin gene sequences have indicated that all butterfly eyes contain ultraviolet-, blue-, and green-sensitive rhodopsins. Some species also contain a fourth or fifth type, related in amino acid sequence to green-sensitive insect rhodopsins, but red shifted in absorbance. By combining electron microscopy, epimicrospectrophotometry, and polymerase chain reaction cloning, we found that the compound eye of Vanessa cardui has the typical ultrastructural features of the butterfly retina but contains only the three common insect rhodopsins. We estimated lambda-max values and relative densities of the rhodopsins in the Vanessa retina (0.72, P530; 0.12, P470; and 0.15, P360) from microspectrophotometric measurements and calculations based on a computational model of reflectance spectra. We isolated three opsin-encoding cDNA fragments that were identified with P530, P470, and P360 by homology to the well-characterized insect rhodopsin families. The retinal mosaic was mapped by opsin mRNA in situ hybridization and found to contain three kinds of ommatidia with respect to their patterns of short wavelength rhodopsin expression. In some ommatidia, P360 or P470 was expressed in R1 and R2 opposed receptor cells; in others, one cell expressed P360, whereas its complement expressed P470. P530 was expressed in the other seven cells of all ommatidia. P470-expressing cells were abundant in the ventral retina but nearly absent dorsally. Our results indicated that there are major differences between the color vision systems of nymphalid and papilionid butterflies: the nymphalid Vanessa has a simpler, trichromatic, system than do the tetrachromatic papilionids that have been studied.",
keywords = "Color vision, Lepidoptera, Nymphalidae, Photoreceptor, Visual pigment",
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AU - Briscoe, Adriana D.

AU - Bernard, Gary D.

AU - Szeto, Allan S.

AU - Nagy, Lisa M

AU - White, Richard H.

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AB - Surveys of spectral sensitivities, visual pigment spectra, and opsin gene sequences have indicated that all butterfly eyes contain ultraviolet-, blue-, and green-sensitive rhodopsins. Some species also contain a fourth or fifth type, related in amino acid sequence to green-sensitive insect rhodopsins, but red shifted in absorbance. By combining electron microscopy, epimicrospectrophotometry, and polymerase chain reaction cloning, we found that the compound eye of Vanessa cardui has the typical ultrastructural features of the butterfly retina but contains only the three common insect rhodopsins. We estimated lambda-max values and relative densities of the rhodopsins in the Vanessa retina (0.72, P530; 0.12, P470; and 0.15, P360) from microspectrophotometric measurements and calculations based on a computational model of reflectance spectra. We isolated three opsin-encoding cDNA fragments that were identified with P530, P470, and P360 by homology to the well-characterized insect rhodopsin families. The retinal mosaic was mapped by opsin mRNA in situ hybridization and found to contain three kinds of ommatidia with respect to their patterns of short wavelength rhodopsin expression. In some ommatidia, P360 or P470 was expressed in R1 and R2 opposed receptor cells; in others, one cell expressed P360, whereas its complement expressed P470. P530 was expressed in the other seven cells of all ommatidia. P470-expressing cells were abundant in the ventral retina but nearly absent dorsally. Our results indicated that there are major differences between the color vision systems of nymphalid and papilionid butterflies: the nymphalid Vanessa has a simpler, trichromatic, system than do the tetrachromatic papilionids that have been studied.

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