Abstract
Recently, in vitro mutation studies have made it possible to predict the wavelengths of maximum absorbance (λmax) of avian UV/violet sensitive visual pigments (SWS1) from the identity of a few key amino acid residues in the opsin gene. Given that the absorbance spectrum of a cone’s visual pigment and of its pigmented oil droplet can be predicted from just the λmax, it may become possible to predict the entire spectral sensitivity of a bird using genetic samples from live birds or museum specimens. However, whilst this concept is attractive, it must be validated to assess the reliability of the predictions of λmax from opsin amino acid sequences. In this paper, we have obtained partial sequences covering three of the known spectral tuning sites in the SWS1 opsin and predicted λmax of all bird species for which the spectral absorbance has been measured using microspectrophotometry. Our results validate the use of molecular data from genomic DNA to predict the gross differences in λmax between the violet- and ultraviolet-sensitive subtypes of SWS1 opsin. Additionally, we demonstrate that a bird, the bobolink Dolichonyx oryzivorus L., can have more than one SWS1 visual pigment in its retina.
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Abbreviations
- λmax :
-
Wavelength of maximum absorbance
- MSP:
-
Microspectrophotometry
- SWS1:
-
Short-wavelength sensitive type one
- SWS2:
-
Short-wavelength sensitive type two
- VS:
-
Violet sensitive
- UVS:
-
Ultraviolet sensitive
References
Beason RC, Loew ER (2008) Visual pigment and oil droplet characteristics of the bobolink (Dolichonyx oryzivorus), a new world migratory bird. Vision Res 48:1–8
Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res 37:2183–2194
Bowmaker JK, Kovach JK, Whitmore AV, Loew ER (1993) Visual pigments and oil droplets in genetically manipulated and carotenoid deprived quail: a microspectrophotometric study. Vision Res 33:571–578
Bowmaker JK, Martin GR (1985) Visual pigments and oil droplets in the penguin, Spheniscus humboldti. J Comp Physiol A 156:71–77
Carvalho LS, Cowing JA, Wilkie SE, Bowmaker JK, Hunt DM (2007) The molecular evolution of avian ultraviolet- and violet-sensitive visual pigments. Mol Biol Evol 24:1843–1852
Clements JF (2007) The Clements checklist of birds of the world, 6th edn. Cornell University Press, Ithaca
Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Stud Behav 29:159–214
Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Visual Neurosci 17:509–528
Das D, Wilkie SE, Hunt DM, Bowmaker JK (1999) Visual pigments and oil droplets in the retina of a passerine bird, the canary Serinus canaria: microspectrophotometry and opsin sequences. Vision Res 39:2801–2815
Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703
Hart NS (2002) Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 205:3925–3935
Hart NS (2004) Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics. J Exp Biol 207:1229–1240
Hart NS, Hunt DM (2007) Avian visual pigments: characteristics, spectral tuning and evolution. Am Nat 169(Suppl):S7–S26
Hart NS, Partridge JC, Bennett ATD, Cuthill IC (2000a) Visual pigments, cone oil droplets and ocular media in four species of estrildid finch. J Comp Physiol A 186:681–694
Hart NS, Partridge JC, Cuthill IC (1998) Visual pigments, oil droplets and cone photoreceptor distribution in the European starling (Sturnus vulgaris). J Exp Biol 201:1433–1446
Hart NS, Partridge JC, Cuthill IC (1999) Visual pigments, cone oil droplets, ocular media and predicted spectral sensitivity in the domestic turkey (Meleagris gallopavo). Vision Res 39:3321–3328
Hart NS, Partridge JC, Cuthill IC, Bennett AT (2000b) Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J Comp Physiol A 186:375–387
Hart NS, Vorobyev M (2005) Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191:381–392
Håstad O, Ernstdotter E, Ödeen A (2005) Ultraviolet vision and foraging in dip and plunge diving birds. Biol Lett 1:306–309
Hunt DM, Carvalho LS, Cowing JA, Parry JW, Wilkie SE, Davies WL, Bowmaker JK (2007) Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol 83:303–310
Jane SD, Bowmaker JK (1988) Tetrachromatic colour vision in the duck (Anas platyrhynchos L.): microspectrophotometry of visual pigments and oil droplets. J Comp Physiol A 162:225–235
Kawamura S, Blow NS, Yokoyama S (1999) Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics 153:1839–1850
Lamb TD (1995) Photoreceptor spectral sensitivities: common shape in the longwave region. Vision Res 35:3083–3091
Lythgoe JN (1979) The ecology of vision. Oxford University Press, Oxford
Maier EJ, Bowmaker JK (1993) Colour vision in the passeriform bird, Leiothrix lutea: correlation of visual pigment absorbance and oil droplet transmission with spectral sensitivity. J Comp Physiol A 172:295–301
Mariani AP (1987) Neuronal and synaptic organization of the outer plexiform layer of the pigeon retina. Am J Anat 179:25–39
Meyer DB (1977) The avian eye and its adaptations. In: Crescitelli F (ed) The visual system in vertebrates, vol. VII/5. Springer, Berlin, pp 549–611
Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–861
Okano T, Kojima D, Fukada Y, Shichida Y, Yoshizawa T (1992) Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc Natl Acad Sci USA 89:5932–5936
Parry JW, Poopalasundaram S, Bowmaker JK, Hunt DM (2004) A novel amino acid substitution is responsible for spectral tuning in a rodent violet-sensitive visual pigment. Biochemistry 43:8014–8020
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386
Shi Y, Radlwimmer FB, Yokoyama S (2001) Molecular genetics and the evolution of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 98:11731–11736
Shi Y, Yokoyama S (2003) Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 100:8308–8313
Stavenga DG, Smits RP, Hoenders BJ (1993) Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Res 33:1011–1017
Walls GL (1942) The vertebrate eye and its adaptive radiation. Hafner, New York
Wilkie SE, Robinson PR, Cronin TW, Poopalasundaram S, Bowmaker JK, Hunt DM (2000) Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments. Biochemistry 39:7895–7901
Wilkie SE, Vissers PM, Das D, DeGrip WJ, Bowmaker JK, Hunt DM (1998) The molecular basis for UV vision in birds: spectral characteristics, cDNA sequence and retinal localization of the UV-sensitive visual pigment of the budgerigar (Melopsittacus undulatus). Biochem J 330:541–547
Yokoyama S, Radlwimmer FB, Blow NS (2000) Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA 97:7366–7371
Acknowledgments
Tissue and DNA samples for this study were kindly provided by Australian Museum, Australian National Wildlife Collection, Borås Zoo, The Burke Museum of Natural History, Department of Animal Ecology, Uppsala University, The Swedish Museum of Natural History, Zoological Museum, University of Copenhagen, Sofia Berlin and Niclas Backström. AÖ was funded by the Swedish Research Council Formas, and Stiftelsen för Zoologisk Forskning (sequencing), NSH by an Australian Research Council QEII Fellowship and OH by the Swedish Research Council (VR). This study complies with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and also with current Swedish law.
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Ödeen, A., Hart, N.S. & Håstad, O. Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments. J Comp Physiol A 195, 167–173 (2009). https://doi.org/10.1007/s00359-008-0395-2
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DOI: https://doi.org/10.1007/s00359-008-0395-2