Journal of Comparative Physiology A

, Volume 195, Issue 4, pp 401–408 | Cite as

Evolution of color vision in pierid butterflies: blue opsin duplication, ommatidial heterogeneity and eye regionalization in Colias erate

Original Paper

Abstract

This paper documents the molecular organization of the eye of the Eastern Pale Clouded Yellow butterfly, Colias erate (Pieridae). We cloned four cDNAs encoding visual pigment opsins, corresponding to one ultraviolet, two blue and one long wavelength-absorbing visual pigments. Duplication of the blue visual pigment class occurs also in another pierid species, Pieris rapae, suggesting that blue duplication is a general feature in the family Pieridae. We localized the opsin mRNAs in the Colias retina by in situ hybridization. Among the nine photoreceptor cells in an ommatidium, R1-9, we found that R3-8 expressed the long wavelength class mRNA in all ommatidia. R1 and R2 expressed mRNAs of the short wavelength opsins in three fixed combinations, corresponding to three types of ommatidia. While the duplicated blue opsins in Pieris are separately expressed in two subsets of R1-2 photoreceptors, one blue sensitive and another violet sensitive, those of Colias appear to be always coexpressed.

Keywords

Visual pigment Photoreceptor Compound eye Insect Color vision 

References

  1. Arikawa K (2003) Spectral organization of the eye of a butterfly Papilio. J Comp Physiol A 189:791–800CrossRefGoogle Scholar
  2. Arikawa K, Stavenga DG (1997) Random array of colour filters in the eyes of butterflies. J Exp Biol 200:2501–2506PubMedGoogle Scholar
  3. Arikawa K, Scholten DGW, Kinoshita M, Stavenga DG (1999) Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool Sci 16:17–24CrossRefGoogle Scholar
  4. Arikawa K, Mizuno S, Kinoshita M, Stavenga DG (2003) Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of a butterfly, Papilio xuthus. J Neurosci 23:4527–4532PubMedGoogle Scholar
  5. Arikawa K, Kinoshita M, Stavenga DG (2004) Color vision and retinal organization in butterflies. In: Prete FR (ed) Complex worlds from simpler nervous system. The MIT Press, Cambridge, pp 193–219Google Scholar
  6. Arikawa K, Wakakuwa M, Qiu X, Kurasawa M, Stavenga DG (2005) Sexual dimorphism of short wavelength photoreceptors in the small white buterfly, Pieris rapae crucivora. J Neurosci 25:5935–5942PubMedCrossRefGoogle Scholar
  7. Braby MF (2006) Molecular phylogenty and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zool J Linn Soc 147:239–275CrossRefGoogle Scholar
  8. Briscoe AD (2000) Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. J Mol Evol 51:110–121PubMedGoogle Scholar
  9. Briscoe AD (2008) Reconstructing the ancestral butterfly eye: a new twist. J Exp Biol 211:1805–1813PubMedCrossRefGoogle Scholar
  10. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510PubMedCrossRefGoogle Scholar
  11. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  12. Fotiadis D, Jastrzebska B, Philippsen A, Muller DJ, Palczewski K, Engel A (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr Opin Struct Biol 16:252–259PubMedCrossRefGoogle Scholar
  13. Frentiu FD, Bernard GD, Sison-Mangus MP, Brower AV, Briscoe AD (2007) Gene duplication is an evolutionary mechanism for expanding spectral diversity in the long-wavelength photopigments of butterflies. Mol Biol Evol 24:2016–2028PubMedCrossRefGoogle Scholar
  14. Giurfa M, Zaccardi G, Vorobyev M (1999) How bees detect coloured targets using different regions of their compound eyes. J Comp Physiol A 185:591–600CrossRefGoogle Scholar
  15. Gordon WC (1977) Microvillar orientation in the retina of the nymphalid butterfly. Z Naturforsch 32c:662–664Google Scholar
  16. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559PubMedCrossRefGoogle Scholar
  17. Homberg U (2004) In search of the sky compass in the insect brain. Naturwiss 91:199–208PubMedCrossRefGoogle Scholar
  18. Kelber A (1999) Ovipositing butterflies use a red receptor to see green. J Exp Biol 202:2619–2630PubMedGoogle Scholar
  19. Kelber A (2006) Invertebrate colour vision. In: Warrant E, Nilsson DE (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 250–290Google Scholar
  20. Kelber A, Pfaff M (1999) True colour vision in the orchard butterfly, Papilio aegeus. Naturwiss 86:221–224CrossRefGoogle Scholar
  21. Kinoshita M, Arikawa K (2000) Colour constancy of the swallowtail butterfly, Papilio xuthus. J Exp Biol 203:3521–3530PubMedGoogle Scholar
  22. Kinoshita M, Shimada N, Arikawa K (1999) Colour vision of the foraging swallowtail butterfly Papilio xuthus. J Exp Biol 202:95–102PubMedGoogle Scholar
  23. Kinoshita M, Takahashi Y, Arikawa K (2008) Simultaneous color contrast in the foraging swallowtail butterfly, Papilio xuthus. J Exp Biol 211:3504–3511PubMedCrossRefGoogle Scholar
  24. Kitamoto J, Sakamoto K, Ozaki K, Mishina Y, Arikawa K (1998) Two visual pigments in a single photoreceptor cell: Identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus. J Exp Biol 201:1255–1261PubMedGoogle Scholar
  25. Kolb G (1978) Zur Rhabdomstruktur des Auges von Pieris brassicae L. (Insecta, Lepidoptera). Zoomorphol 91:191–200CrossRefGoogle Scholar
  26. Labhart T, Meyer EP (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47:368–379PubMedCrossRefGoogle Scholar
  27. Mazzoni EO, Celik A, Wernet MF, Vasiliauskas D, Johnston RJ, Cook TA, Pichaud F, Desplan C (2008) Iroquois complex genes induce co-expression of rhodopsins in Drosophila. PLoS Biol 6:e97PubMedCrossRefGoogle Scholar
  28. Prinster SC, Hague C, Hall RA (2005) Heterodimerization of G protein-coupled receptors: specificity and functional significance. Pharmacol Rev 57:289–298PubMedCrossRefGoogle Scholar
  29. Qiu X, Arikawa K (2003a) Polymorphism of red receptors: Sensitivity spectra of proximal photoreceptors in the small white butterfly, Pieris rapae crucivora. J Exp Biol 206:2787–2793PubMedCrossRefGoogle Scholar
  30. Qiu X, Arikawa K (2003b) The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly, Pieris rapae crucivora. J Comp Physiol A 189:81–88Google Scholar
  31. Rossel S (1989) Polarization sensitivity in compound eyes. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin, pp 298–316Google Scholar
  32. Salcedo E, Zheng L, Phistry M, Bagg EE, Britt SG (2003) Molecular basis for ultraviolet visioin in invertebrates. J Neurosci 23:10873–10878PubMedGoogle Scholar
  33. Sauman I, Briscoe AD, Zhu H, Shi D, Froy O, Stalleicken J, Yuan Q, Casselman A, Reppert SM (2005) Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46:457–467PubMedCrossRefGoogle Scholar
  34. Sison-Mangus MP, Bernard GD, Lampel J, Briscoe AD (2006) Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes. J Exp Biol 209:3079–3090PubMedCrossRefGoogle Scholar
  35. Stavenga DG (2002) Reflections on colourful ommatidia of butterfly eyes. J Exp Biol 205:1077–1085PubMedGoogle Scholar
  36. Stavenga DG, Kinoshita M, Yang E-C, Arikawa K (2001) Retinal regionalization and heterogeneity of butterfly eyes. Naturwissenschaften 88:477–481PubMedCrossRefGoogle Scholar
  37. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  38. Wakakuwa M, Stavenga DG, Kurasawa M, Arikawa K (2004) A unique visual pigment expressed in green, red and deep-red receptors in the eye of the small white butterfly, Pieris rapae crucivora. J Exp Biol 207:2803–2810PubMedCrossRefGoogle Scholar
  39. Wakakuwa M, Kurasawa M, Giurfa M, Arikawa K (2005) Spectral heterogeneity of honeybee ommatidia. Naturwiss 92:464–467PubMedCrossRefGoogle Scholar
  40. Wakakuwa M, Stavenga DG, Arikawa K (2006) Spectral organization of ommatidia in flower-visiting insects. Photochem Photobiol 83:27–34CrossRefGoogle Scholar
  41. Yagi N, Koyama N (1963) The compound eye of Lepidoptera. Approach from organic evolution, MaruzenGoogle Scholar
  42. Zaccardi G, Kelber A, Sison-Mangus MP, Briscoe AD (2006) Color discrimination in the red range with only one long-wavelength sensitive opsin. J Exp Biol 209:1944–1955PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Hiroko Awata
    • 1
  • Motohiro Wakakuwa
    • 1
    • 2
  • Kentaro Arikawa
    • 1
  1. 1.Laboratory of NeuroethologySokendai (The Graduate University for Advanced Science)HayamaJapan
  2. 2.Department of Biophysics, Graduate School of ScienceKyoto UniversityKyotoJapan

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