How parrots see their colours: Novelty in the visual pigments of Platycercus elegans

Journal of Experimental Biology

Volumn 216, Issue 23, 2013, Pages 4454-4461

  Knott, Ben ^a,b   Davies, Wayne I L ^c,d   Carvalho, Livia S ^c   Berg, Mathew L ^a,b   Buchanan, Katherine L ^b,e   Bowmaker, James K ^c   Bennett, Andrew T D ^a,b   Hunt, David M ^c,d  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b DEAKIN UNIVERSITY   (Australia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Alternative splicing; Microspectrophotometry; Opsin; Parrot; Platycercus elegans; Visual pigment

Indexed keywords

AVIAN PROTEIN; OPSIN; VISUAL PIGMENT;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; COLOR; COLOR VISION; GENETICS; MICROSPECTROPHOTOMETRY; MOLECULAR GENETICS; PARROT; PHYLOGENY; PHYSIOLOGY; PLATYCERCUS ELEGANS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

ALTERNATIVE SPLICING; MICROSPECTROPHOTOMETRY; OPSIN; PARROT; PLATYCERCUS ELEGANS; VISUAL PIGMENT;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; AVIAN PROTEINS; COLOR; COLOR VISION; MOLECULAR SEQUENCE DATA; OPSINS; PARROTS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN;

EID: 84889007076     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.094136     Document Type: Article

References (66)

1. al-Ubaidi, M. R., Pittler, S. J., Champagne, M. S., Triantafyllos, J. T., McGinnis, J. F. and Baehr, W. (1990). Mouse opsin. Gene structure and molecular basis of multiple transcripts. J. Biol. Chem. 265, 20563-20569.
2. Applebury, M. L., Antoch, M. P., Baxter, L. C., Chun, L. L., Falk, J. D., Farhangfar, F., Kage, K., Krzystolik, M. G., Lyass, L. A. and Robbins, J. T. (2000). The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513-523.
3. Bennett, A. T. D. and Thery, M. (2007). Avian color vision and coloration: multidisciplinary evolutionary biology. Am. Nat. 169, S1-S6.
4. Bennett, A. T. D., Cuthill, I. C. and Norris, K. J. (1994). Sexual selection and the mismeasure of color. Am. Nat. 144, 848-860.
5. Berg, M. L. and Bennett, A. T. D. (2010). The evolution of plumage colouration in parrots: a review. Emu 110, 10-20.
6. Bowmaker, J. K., Kovach, J. K., Whitmore, A. V. and Loew, E. R. (1993). Visual pigments and oil droplets in genetically manipulated and carotenoid deprived quail: a microspectrophotometric study. Vision Res. 33, 571-578.
7. Bowmaker, J. K., Heath, L. A., Wilkie, S. E. and Hunt, D. M. (1997). Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res. 37, 2183-2194.
8. Carvalho, L. S., Knott, B., Berg, M. L., Bennett, A. T. D. and Hunt, D. M. (2011). Ultraviolet-sensitive vision in long-lived birds. Proc. Biol. Sci. 278, 107-114.
9. Concepcion, F., Mendez, A. and Chen, J. (2002). The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vision Res. 42, 417-426.
10. Cowing, J. A., Poopalasundaram, S., Wilkie, S. E., Robinson, P. R., Bowmaker, J. K. and Hunt, D. M. (2002). The molecular mechanism for the spectral shifts between vertebrate ultraviolet- and violet-sensitive cone visual pigments. Biochem. J. 367, 129-135.
11. Davies, W. L., Cowing, J. A., Carvalho, L. S., Potter, I. C., Trezise, A. E., Hunt, D. M. and Collin, S. P. (2007). Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J. 21, 2713- 2724.
12. Davies, W. L., Carvalho, L. S. and Hunt, D. M. (2009a). Protocol for SPLICE: a technique for generating in vitro spliced coding sequences from genomic DNA. In BioTechniques Protocol Guide 01/2009. New York: Informa BioSciences.
13. Davies, W. L., Cowing, J. A., Bowmaker, J. K., Carvalho, L. S., Gower, D. J. and Hunt, D. M. (2009b). Shedding light on serpent sight: the visual pigments of henophidian snakes. J. Neurosci. 29, 7519-7525.
14. Davies, W. L., Hankins, M. W. and Foster, R. G. (2010). Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem. Photobiol. Sci. 9, 1444- 1457.
15. Davies, W. I., Zheng, L., Hughes, S., Tamai, T. K., Turton, M., Halford, S., Foster, R. G., Whitmore, D. and Hankins, M. W. (2011). Functional diversity of melanopsins and their global expression in the teleost retina. Cell. Mol. Life Sci. 68, 4115-4132.
16. Davies, W. I., Collin, S. P. and Hunt, D. M. (2012). Molecular ecology and adaptation of visual photopigments in craniates. Mol. Ecol. 21, 3121-3158.
17. Endler, J. A. (1992). Signals, signal conditions, and the direction of evolution. Am. Nat. 139, S125-S153.
18. Endler, J. A. and McLellan, T. (1988). The processess of evolution - toward a newer synthesis. Annu. Rev. Ecol. Syst. 19, 395-421.
19. Forshaw, J. and Cooper, W. T. (2002). Australian Parrots. Robina, QLD, Australia: Robina Press.
20. Goldsmith, T. H. and Butler, B. K. (2005). Color vision of the budgerigar (Melopsittacus undulatus): hue matches, tetrachromacy, and intensity discrimination. J. Comp. Physiol. A 191, 933-951.
21. Govardovskii, V. I., Fyhrquist, N., Reuter, T., Kuzmin, D. G. and Donner, K. (2000). In search of the visual pigment template. Vis. Neurosci. 17, 509-528.
22. Hart, N. S. and Hunt, D. M. (2007). Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat. 169 Suppl. 1, S7-S26.
23. Hart, N. S., Lisney, T. J. and Collin, S. P. (2006). Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity. J. Exp. Biol. 209, 4776-4787.
24. Higgins, D. G., Thompson, J. D. and Gibson, T. J. (1996). Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266, 383-402.
25. Hunt, D. M., Carvalho, L. S., Cowing, J. A., Parry, J. W., Wilkie, S. E., Davies, W. L. and Bowmaker, J. K. (2007). Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem. Photobiol. 83, 303-310.
26. Hunt, D. M., Carvalho, L. S., Cowing, J. A. and Davies, W. L. (2009). Evolution and spectral tuning of visual pigments in birds and mammals. Philos. Trans. R. Soc. B 364, 2941-2955.
27. Irwin, D. E. and Irwin, J. H. (2002). Circular overlaps: rare demonstrations of speciation. Auk 119, 596-602.
28. Joseph, L., Dolman, G., Donnellan, S., Saint, K. M., Berg, M. L. and Bennett, A. T. D. (2008). Where and when does a ring start and end? Testing the ring-species hypothesis in a species complex of Australian parrots. Proc. Biol. Sci. 275, 2431- 2440.
29. Kawamura, S., Blow, N. S. and Yokoyama, S. (1999). Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics 153, 1839-1850.
30. Knott, B., Berg, M. L., Morgan, E. R., Buchanan, K. L., Bowmaker, J. K. and Bennett, A. T. D. (2010). Avian retinal oil droplets: dietary manipulation of colour vision? Proc. Biol. Sci. 277, 953-962.
31. Knott, B., Bowmaker, J. K., Berg, M. L. and Bennett, A. T. D. (2012). Absorbance of retinal oil droplets of the budgerigar: sex, spatial and plumage morph-related variation. J. Comp. Physiol. A 198, 43-51.
32. Kostenis, E. (2002). Potentiation of GPCR-signaling via membrane targeting of G protein alpha subunits. J. Recept. Signal Transduct. Res. 22, 267-281.
33. Liebman, P. A. and Entine, G. (1964). Sensitive low-light-level microspectrophotometer: detection of photosensitive pigments of retinal cones. J. Opt. Soc. Am. 54, 1451-1459.
34. Lin, S. W., Kochendoerfer, G. G., Carroll, K. S., Wang, D., Mathies, R. A. and Sakmar, T. P. (1998). Mechanisms of spectral tuning in blue cone visual pigments. Visible and raman spectroscopy of blue-shifted rhodopsin mutants. J. Biol. Chem. 273, 24583-24591.
35. Lythgoe, J. N. (1979). The Ecology of Vision. Oxford: Oxford University Press.
36. Maeda, A., Okano, K., Park, P. S., Lem, J., Crouch, R. K., Maeda, T. and Palczewski, K. (2010). Palmitoylation stabilizes unliganded rod opsin. Proc. Natl. Acad. Sci. USA 107, 8428-8433.
37. Marchetti, K. (1993). Dark habitats and bright birds illustrate the role of the environment in species divergence. Nature 362, 149-152.
38. Mayr, E. (1963). Animal Species and Evolution. Cambridge, MA: Belknap Press of Harvard University Press.
39. Mazelova, J., Astuto-Gribble, L., Inoue, H., Tam, B. M., Schonteich, E., Prekeris, R., Moritz, O. L., Randazzo, P. A. and Deretic, D. (2009). Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 28, 183-192.
40. Mollon, J. D., Bowmaker, J. K. and Jacobs, G. H. (1984). Variations of color-vision in a new world primate can be explained by polymorphism of retinal photopigments. Proc. R. Soc. B 222, 373-399.
41. Nathans, J. (1990). Determinants of visual pigment absorbance: role of charged amino acids in the putative transmembrane segments. Biochemistry 29, 937-942.
42. Nathans, J., Piantanida, T. P., Eddy, R. L., Shows, T. B. and Hogness, D. S. (1986). Molecular genetics of inherited variation in human color vision. Science 232, 203-210.
43. Ohguro, H., Palczewski, K., Ericsson, L. H., Walsh, K. A. and Johnson, R. S. (1993). Sequential phosphorylation of rhodopsin at multiple sites. Biochemistry 32, 5718-5724.
44. Okano, T., Kojima, D., Fukada, Y., Shichida, Y. and 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.
45. Parry, J. W. L., Carleton, K. L., Spady, T., Carboo, A., Hunt, D. M. and Bowmaker, J. K. (2005). Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Curr. Biol. 15, 1734-1739.
46. Pearn, S. M., Bennett, A. T. D. and Cuthill, I. C. (2003a). The role of ultraviolet-A reflectance and ultraviolet-A induced fluorescence in the appearance of budgerigar plumage: insights from spectrofluorometry and reflectance spectrophotometry. Proc. Biol. Sci. 270, 859-865.
47. Pearn, S. M., Bennett, A. T. D. and Cuthill, I. C. (2003b). The role of ultraviolet-A reflectance and ultraviolet-A-induced fluorescence in budgerigar mate choice. Ethology 109, 961-970.
48. Ribot, R. F. H., Berg, M. L., Buchanan, K. L., Komduer, J., Joseph, L. and Bennett, A. T. D. (2009). Does the ring species concept predict vocal variation in the crimson rosella, Platycercus elegans, complex? Anim. Behav. 77, 581-593.
49. Ribot, R. F. H., Berg, M. L., Buchanan, K. L. and Bennett, A. T. D. (2011). Fruitful use of bioacoustic alarm stimuli as a deterrent for crimson rosellas (Platycercus elegans). Emu 111, 360-367.
50. Ribot, R. F. H., Buchanan, K. L., Endler, J. A., Joseph, L., Bennett, A. T. D. and Berg, M. L. (2012). Learned vocal variation is associated with abrupt cryptic genetic change in a parrot species complex. PLoS ONE 7, e50484.
51. Ribot, R. F. H., Berg, M. L., Buchanan, K. L. and Bennett, A. T. D. (2013). Is there variation in the response to contact call playbacks across the hybrid zone of the parrot Platycercus elegans? J. Avian Biol. 44, 399-407.
52. Romero, G., von Zastrow, M. and Friedman, P. A. (2011). Role of PDZ proteins in regulating trafficking, signaling, and function of GPCRs: means, motif, and opportunity. Adv. Pharmacol. 62, 279-314.
53. Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
54. Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512-526.
55. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
56. Vorobyev, M. (2003). Coloured oil droplets enhance colour discrimination. Proc. R. Soc. B 270, 1255-1261.
57. Vorobyev, M., Osorio, D., Bennett, A. T. D., Marshall, N. J. and Cuthill, I. C. (1998). Tetrachromacy, oil droplets and bird plumage colours. J. Comp. Physiol. A 183, 621-633.
58. Whitmore, A. V. and Bowmaker, J. K. (1989). Seasonal variation in cone sensitivity and short-wave absorbing visual pigments in the rudd Scadinius erythrophythalmus. J. Comp. Physiol. A 166, 103-115.
59. Wilkie, S. E., Vissers, P., Das, D., deGrip, W. J., Bowmaker, J. K. and Hunt, D. M. (1997). Short-wave sensitive visual pigments from birds: The ultraviolet-sensitive opsin from budgerigar (Melopsittacus undulatus). Invest. Ophthalmol. Vis. Sci. 38, 1046.
60. Wistow, G., Bernstein, S. L., Wyatt, M. K., Ray, S., Behal, A., Touchman, J. W., Bouffard, G., Smith, D. and Peterson, K. (2002). Expressed sequence tag analysis of human retina for the NEIBank Project: retbindin, an abundant, novel retinal cDNA and alternative splicing of other retina-preferred gene transcripts. Mol. Vis. 8, 196- 204.
61. Yokoyama, S. (2000a). Molecular evolution of vertebrate visual pigments. Prog. Retin. Eye Res. 19, 385-419.
62. Yokoyama, S. (2000b). Color vision of the coelacanth (Latimeria chalumnae) and adaptive evolution of rhodopsin (RH1) and rhodopsin-like (RH2) pigments. J. Hered. 91, 215-220.
63. Yokoyama, S. and Tada, T. (2003). The spectral tuning in the short wavelengthsensitive type 2 pigments. Gene 306, 91-98.
64. Yokoyama, S. and Tada, T. (2010). Evolutionary dynamics of rhodopsin type 2 opsins in vertebrates. Mol. Biol. Evol. 27, 133-141.
65. Yokoyama, S., Blow, N. S. and Radlwimmer, F. B. (2000). Molecular evolution of color vision of zebra finch. Gene 259, 17-24.
66. Yokoyama, S., Tada, T. and Yamato, T. (2007). Modulation of the absorption maximum of rhodopsin by amino acids in the C-terminus. Photochem. Photobiol. 83, 236-241. Council