Opsin gene duplication and divergence in ray-finned fish

Molecular Phylogenetics and Evolution

Volumn 62, Issue 3, 2012, Pages 986-1008

  Rennison, Diana J ^a,b   Owens, Gregory L ^a,b   Taylor, John S ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Gene duplication; Opsins; Phylogenies; Ray finned fish; Vision

Indexed keywords

OPSIN;

ANIMAL; CHEMISTRY; CLASSIFICATION; GENE CONVERSION; GENE DUPLICATION; GENETICS; PHYLOGENY; PSEUDOGENE; REVIEW; SKATES (FISH);

ANIMALS; GENE CONVERSION; GENE DUPLICATION; OPSINS; PHYLOGENY; PSEUDOGENES; SKATES (FISH);

ACTINOPTERYGII; DANIO RERIO; PISCES;

EID: 84856258901     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.11.030     Document Type: Review

References (138)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D. Basic Local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Alvares C.E. On the origin of arrestin and rhodopsin. BMC Evol. Biol. 2008, 8:222.
3. Amores A., Force A., Yan Y.L., Joly L., Amemiya C., Fritz A., Ho R.K., Langeland J., Prince V., Wang Y.-L., Westerfield M., Ekker M., Postlethwait J.H. Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
4. Anisimova M., Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 2006, 55:539-552.
5. Anisimova M., Yang Z. Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. Mol. Biol. Evol. 2007, 24:1219-1228.
6. Anisimova M., Bielawski J.P., Yang Z. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol. Biol. Evol. 2001, 18:1585-1592.
7. Archer S., Hope A., Partridge J.C. The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proc. Biol. Sci. 1995, 262:289-295.
8. Arendt D., Tessmar-Raible K., Snyman H., Adriaan W.D., Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 2004, 306:869-871.
9. Bielawski J.P., Yang Z. Positive and negative selection in the DAZ gene family. Mol. Biol. Evol. 2001, 18:523-529.
10. Blackshaw S., Snyder S.H. Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J. Neurosci. 1997, 17:8083-8092.
11. Bowmaker J.K., Knowles A. The visual pigments and oil droplets of the chicken, Gallus gallus. Vis. Res. 1977, 17:755-764.
12. Brosius J. RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 1999, 238:115-134.
13. Cameron D.A., Pugh E.N. Double cones as a basis for a new type of polarization vision in vertebrates. Nature 1991, 353:161-164.
14. Collin S.P., Trezise A.E. The origins of colour vision in vertebrates. Clin. Exp. Optom. 2004, 87:217-223.
15. Cowing J.A., Poopalasundaram S., Wilkie S.E., Bowmaker J.K., Hunt D.M. Spectral tuning and evolution of short wave-sensitive cone pigments in cottoid fish from Lake Baikal. Biochemistry 2002, 41:6019-6025.
16. Cowing, J.A., Arrese, C.A., Davies, W.L., Beazley, L.D., Hunt, D.M., 2008. Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus).
17. Davies W.L., Cowing J.A., Carvalho L.S., Potter I.C., Trezise A.E., Hunt D.M., Collin S.P. Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J. 2007, 21:2713-2724.
18. Davies W.L., Collin S.P., Hunt D.M. Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol. Biol. Evol. 2009, 26:1803-1809.
19. Davies W.L., Carvalho L.S., Tay B.H., Brenner S., Hunt D.M., Venkatesh B. Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res. 2009, 19:415-426.
20. Douglas R.H., Partridge J.C. On the visual pigments of deep-sea fish. J. Fish. Biol. 1997, 50:68-85.
21. Douglas R.H., Partridge J.C., Marshall N.J. The eyes of deep-sea fish I. Lens pigmentation, tapeta and visual pigments. Prog. Ret. Eye Res. 1998, 17:597-636.
22. Eakin R.M. Evolution of photoreceptors. Cold. SH. Q. B. 1965, 30:363-370.
23. Endler J.A. Natural Selection in the Wild 1986, Princeton Univ. Press, Princeton, NJ.
24. Falk, J.D., Applebury, M.L., 1988. The molecular genetics of photoreceptor cells. In: Osborne, N., Chader, G.J. (Eds.), Progress in Retinal Research, vol. 7. pp. 89-112.
25. Fay J.C., Wu C.-I. Sequence divergence, functional constraint, and selection in protein evolution. Annu. Rev. Genomics. Hum. Genet. 2003, 4:213-235.
26. Felsenstein J. Confidence limits on phylogenies: an approach using bootstrap. Evolution 1985, 39:783-791.
27. Fredriksson R., Schiöth H.B. The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol. Pharmacol. 2005, 67:1414-1425.
28. Fredriksson R., Lagerström M.C., Lundin L.-G., Schiöth H.B. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 2003, 63:1256-1272.
29. Fuller R.C., Carleton K.L., Fadool J.M., Spady T.C., Travis J. Genetic and environmental variation in the visual properties of bluefin killifish, Lucania goodei. J. Evol. Biol. 2005, 18:516-523.
30. Gojobori J., Innan H. Potential of fish opsin gene duplications to evolve new adaptive functions. Trends Genet. 2009, 25:198-202.
31. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
32. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. 1999, 41:95-98.
33. Haussler D., O'Brien S.J., Ryder O.A., Barker F.K., Clamp M., Crawford A.J., Hanner R., Hanotte O., Johnson W.E., McGuire J.A., et al. Genome 10K: a proposal to obtain whole-genome sequence for 10,000 vertebrate species. J. Hered. 2009, 100:659-674.
34. Hisatomi O., Satoh T., Tokunaga F. The primary structure and distribution of killifish visual pigments. Vis. Res. 1997, 37:3089-3096.
35. Hoegg S., Brinkmann H., Taylor J.S., Meyer A. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J. Mol. Evol. 2004, 59:190-203.
36. Hoffmann M., Tripathi N., Henz S.R., Lindholm A.K., Weigel D., Breden F., Dreyer C. Opsin gene duplication and diversification in the guppy, a model for sexual selection. Proc. Roy. Soc. B 2007, 274:33-42.
37. Hofmann C.M., Carleton K.L. Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish. Integr. Comp. Biol. 2009, 49:630-643.
38. Hope A.J., Partridge J.C., Hayes P.K. Switch in rod opsin gene expression in the European eel, Anguilla anguilla (L.). Proc. Roy. Soc. B 1998, 265:869-874.
39. Hordijk W., Gascuel O. Improving the efficiency of SPR moves in phylogenetic tree search methods based on maximum likelihood. Bioinformatics 2005, 21:4338-4347.
40. Hughes A.L., Friedman R. Codon-based tests of positive selection, branch lengths, and the evolution of mammalian immune system genes. Immunogenetics 2008, 60:495-506.
41. Hunt D.M., Fitzgibbon J., Slobodyanyuk S.J., Bowmkaer J.K., Dulai K.S. Molecular evolution of the cottoid fish endemic to lake Baikal deduced from nuclear DNA evidence. Mol. Phylogenet. Evol. 1997, 8:415-422.
42. Hurley I.A., Mueller R.L., Dunn K.A., Schmidt E.J., Friedman M., Ho R.K., Prince V.E., Yang Z., Thomas M.G., Coates M.I. A new time-scale for ray-finned fish evolution. Proc. Roy. Soc. B 2007, 274:489-498.
43. Ibbotson R.E., Hunt D.M., Bowmaker J.K., Mollon J.D. Sequence divergence and copy number of the middle- and long-wave photopigment genes in old world monkeys. Proc. Roy. Soc. B 1992, 247:145-154.
44. Jacobs G.H., Neitz M., Deegan J.F., Neitz J. Trichromatic color vision in new world monkeys. Nature 1996, 382:156-158.
45. Johnson R.L., Grant K.B., Zankel T.C., Boehm M.F., Merbs S.L., Nathans J., Nakanishi K. Cloning and expression of goldfish opsin sequences. Biochemistry 1993, 32:208-214.
46. Kasai A., Oshima N. Light-sensitive motile iridophores and visual pigments in the neon tetra, Paracheirodon innesi. Zool. Sci. 2006, 23:815-819.
47. Kawamura S., Yokoyama S. Paralogous origin of the rhodopsin-like opsin genes in lizards. J. Mol. Evol. 1995, 40:594-600.
48. Kawamura S., Yokoyama S. Phylogenetic relationships among short wavelength-sensitive opsins of American Chameleon (Anolis carolinensis) and other vertebrates. Vis. Res. 1996, 36:2797-2804.
49. Kondrashov F.A., Rogozin I.B., Wolf Y.I., Koonin E.V. Selection in the evolution of gene duplicates. Genome Biol. 2002, 3. 0008.1-0008.9.
50. Kozmik Z., Ruzickova J., Jonasova K., Matsumoto Y., Volapensky P., Kozmikova I., Strnad H., Kawamura S., Piatigorsky J., Paces V., Vlcek C. Assembly of cnidarian camera-type eye from vertebrate-like components. Proc. Natl. Acad. Sci. USA 2008, 105:8989-8993.
51. Kühne, W., 1879. Chemische Vorgänge in der Netzhaut. In: Hermann, L., Handbuch der physiologie, vol. 3, pp. 235-342.
52. Kuraku S., Meyer A., Kuratani S. Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after?. Mol. Biol. Evol. 2009, 26:47-59.
53. Larhammar D., Nordström K., Larsson T.A. Evolution of vertebrate rod and cone phototransduction genes. Proc. Roy. Soc. B 2009, 364:2867-2880.
54. Laver C.R.J., Taylor J.S. RT-qPCR reveals opsin gene upregulation associated with age and sex in guppies (Poecilia reticulata) - a species with color-based sexual selection and 11 visual-opsin genes. BMC Evol. Biol. 2011, 11:81.
55. Levine J.S., MacNichol E.F. Visual pigments in teleost fishes: effects of habitat, microhabitat, and behaviour on visual system evolution. Sens. Process. 1979, 3:95-131.
56. Li Z., Gan X., He S. Distinct evolutionary patterns between two duplicated color vision genes within cyprinid fishes. J. Mol. Evol. 2009, 69:346-359.
57. Littlepage J.L. Oceanographic investigations in McMurdo Sound, Antarctica. Biology of the Antarctic Seas II. Antarct. Res. Ser. 1965, vol. 5:1-37. American Geophysical Union, Washington.
58. Loew E.R., Lythgoe J.N. The ecology of cone pigments in teleost fishes. Vis. Res. 1978, 18:715-722.
59. Matsumoto Y., Fukamachi S., Mitani H., Kawamura S. Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 2006, 371:268-278.
60. Max M., McKinnon P.J., Seidenman K.J., Barrett R.K., Applebury M.L., Takahashi J.S., Margolskee R.F. Pineal opsin: a nonvisual opsin expressed in chick pineal. Science 1995, 267:1502-1506.
61. McCormack W.T., Tjoelker L.W., Thompson C.B. Avian B-cell development: generation of an immunoglobulin repertoire by gene conversion. Annu. Rev. Immunol. 1991, 9:219-241.
62. Miller R.G. Simultaneous Statistical Inference 1981, Springer-Verlag, New York.
63. Minamoto T., Shimizu I. Molecular cloning of cone opsin genes and their expression in the retina of a smelt, Ayu (Plecoglossus altivelis, Teleostei). Comp. Biochem. Phys. B 2005, 140:197-205.
64. Morrow J.M., Lazic S., Chang B.S.W. A novel rhodopsin-like gene expressed in zebrafish retina. Visual Neurosci. 2011, 28:325-335.
65. Nakamura I. Trichiuridae. Peces sables, cintillas. Guia FAO para Identification de Especies para lo Fines de la Pesca Pacifico Centro-Oriental 1995, 1638-1642. FAO, Rome. W. Fischer, F. Krupp, W. Schneider, C. Sommer, K.E. Carpenter, V. Niem (Eds.).
66. Nakamura I., Parin N.V. FAO Species Catalogue. An annotated and Illustrated Catalogue of the Snake Mackerels, Snoeks, Escolars, Gemfishes, Sackfishes, Domine, Oilfish, Cutlassfishes, Scabbardfishes, Hairtails, and Frostfishes Known to Date 1993, vol. 15. FAO, Rome, pp. 125-136.
67. Nathans J. Determinants of visual pigment absorbance: role of charged amino acids in the putative transmembrane segments. Biochemistry 1990, 29:937-942.
68. Nathans J., Hogness D.S. Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell 1983, 34:807-814.
69. Nathans J., Hogness D.S. Isolation and nucleotide sequence of the gene encoding human rhodopsin. Proc. Natl. Acad. Sci. USA 1984, 81:4851-4855.
70. Nathans J., Thomas D., Hogness D.S. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 1986, 232:193-202.
71. Neafsey D.E., Hartl D.L. Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon pufferfish lineages. Gene 2005, 350:161-171.
72. Nelson J.S. Fishes of the World 2006, Wiley, New York. fourth ed.
73. Nielsen R., Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 1998, 148:929-936.
74. Nozawa M., Suzuki Y., Nei M. Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc. Natl. Acad. Sci. USA 2009, 106:6700-6705.
75. Okamura K., Nakai K. Retrotransposition as a source of new promoters. Mol. Biol. Evol. 2008, 25:1231-1238.
76. Okano T., Kojima D., Fukada Y., Shichida Y., Yoshizawa T. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc. Natl. Acad. Sci. USA 1992, 89:5932-5936.
77. O'Quin K.E., Hofmann C.M., Hofmann H.A., Carleton K.L. Parallel evolution of opsin gene expression in African cichlid fishes. Mol. Biol. Evol. 2010, 27:2839-2854.
78. O'Quin K.E., Smith D., Naseer Z., Schulte J., Engel S.D., Loh Y.-H., Streelman J.T., Boore J.L., Carleton K.L. Divergence in cis-regulatory sequences surrounding the opsin gene arrays of African cichlid fishes. BMC Evol. Biol. 2011, 11:120.
79. Osorio D., Vorobyev M. Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc. Roy. Soc. B 2005, 272:1745-1752.
80. Osorio D., Vorobyev M. A review of the evolution of animal colour vision and visual communication signals. Vis. Res. 2008, 48:2042-2051.
81. Owens G.L., Windsor D.J., Mui J., Taylor J.S. A fish eye out of water: ten visual opsins in the four-eyed fish, Anableps anableps. PloS one 2009, 4:e5970.
82. Owens G.L., Rennison D.J., Allison W.T., Taylor J.S. In the four-eyed fish (Anableps anableps), the regions of the retina exposed to aquatic and aerial light do not express the same set of opsin genes. Biol. Lett. 2011.
83. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., Le Trong I., Teller D.C., Okada T., Stenkamp R.E., Yamamoto M., Miyano M. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 2000, 289:739-745.
84. Pankhurst N.W., Montgomery J.C. Visual function in four Antarctic nototheniid fishes. J. Exp. Biol. 1989, 142:311-324.
85. Park J.H., Scheerer P., Hofmann K.P., Choe H.W., Ernst O.P. Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 2008, 454:183-187.
86. Partridge J.C., Shand J., Archer S.N., Lythgoe J.N., van Groningen-Luyben W.A. Interspecific variation in the visual pigments of deep-sea fishes. J. Comp. Phys. A 1989, 164:513-529.
87. Perovich D.K., Longacre J., Barber D.G., Maffione R.A., Cota G.F., Mobley C.D., Gow A.J., Onstott R.G., Grenfell T.C., Pegau W.S., Laundry M., Roesler C.S. Field observations of the electromagnetic properties of first-year sea ice. IEEE Trans. Geosci. Remote 1998, 36:1705-1715.
88. Pignatelli V., Champ C., Marshall J., Vorobyev M. Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biol. Lett. 2010, 6:537-539.
89. Plachetzki D.C., Serb J.M., Oakley T.H. New insights into the evolutionary history of photoreceptor cells. TREE 2005, 20:465-467.
90. Pointer M.A., Cheng C.H., Bowmaker J.K., Parry J.W., Soto N., Jeffery G., Cowing J.A., Hunt D.M. Adaptations to an extreme environment: retinal organisation and spectral properties of photoreceptors in Antarctic notothenioid fish. J. Exp. Biol. 2005, 208:2363-2376.
91. Posada D., Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
92. Pride, D.T., 2000. SWAAP Version 1.0.3-Sliding Windows Alignment Analysis Program: A Tool for Analyzing Patterns of Substitutions and Similarity in Multiple Alignments.
93. Raes J., Van de Peer Y. Gene duplication, the evolution of novel gene functions, and detecting functional divergence of duplicates in silico. Appl. Bioinformat. 2003, 2:91-101.
94. Raymond P.A., Barthel L.K., Rounsifer M.E., Sullivan S.A., Knight J.K. Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cones. Vis. Res. 1993, 10:1161-1174.
95. Register A.R., Yokoyama R., Yokoyama S. Multiple origins of green-sensitive opsins in fish. J. Mol. Evol. 1994, 39:268-273.
96. Rennison D.J., Owens G.L., Allison W.T., Taylor J.S. Intra-retinal variation of opsin gene expression in the guppy (Poecilia reticulata). J. Exp. Biol. 2011, 214:3248-3254.
97. Reyniers E., van Thienen M.N., Meire F., de Boulle K., Devries K., Kestelijn P., Willems P.J. Gene conversion between red and defective green opsin gene in blue cone monochromacy. Genomics 1995, 29:323-328.
98. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406.
99. Sakmar T.P., Franke R.R., Khorana H.G. Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. USA 1989, 86:8309-8313.
100. Scheerer P., Park J.H., Hildebrand P.W., Kim Y.J., Krauss N., Choe H.W., Hofmann K.P., Ernst O.P. Crystal structure of opsin in its G-protein-interacting conformation. Nature 2008, 455:497-502.
101. Shand J., Davies W.L., Thomas N., Balmer L., Cowing J.A., Pointer M., Carvalho L.S., Trezise A.E., Collin S.P., Beazley L.D., Hunt D.M. The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, Acanthopagrus butcheri. J. Exp. Biol. 2008, 211:1495-1503.
102. Shi Y., Radlwimmer F.B., Yokoyama S. Molecular genetics and the evolution of ultraviolet vision in vertebrates. Proc. Natl. Acad. Sci. USA 2001, 98:11731-11736.
103. Simpson G.G. The Major Features of Evolution 1953, Columbia Univ. Press, New York.
104. Spady T.C. Cichlids as a Model for the Evolution of Visual Sensitivity 2006, University of New Hampshire, Durham, NH.
105. Spady T.C., Parry J.W., Robinson P.R., Hunt D.M., Bowmaker J.K., Carleton K.L. Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Mol. Biol. Evol. 2006, 23:1538-1547.
106. Suga H., Schmid V., Gehring W.J. Evolution and functional diversity of jellyfish opsins. Curr. Biol. 2008, 18:51-55.
107. Swofford D.L. PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0 b10 2002, Sinauer Associates, Sunderland, MA.
108. Takechi M., Kawamura S. Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. J. Exp. Biol. 2005, 208:1337-1345.
109. Tamura K., Kumar S. Evolutionary distance estimation under heterogeneous substitution pattern among lineages. Mol. Biol. Evol. 2002, 19:1727-1736.
110. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10:512-526.
111. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
112. Tang F., Barbacioru C., Wang Y., Nordman E., Lee C., Xu N., Wang X., Bodea J., Tuch B.B., Siddiqui A., Lao K., Surani M.A. MRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods 2009, 6:377-382.
113. Tansley K. The regeneration of visual purple: its relation to dark adaptation and night blindness. J. Physiol. 1931, 71:442-458.
114. Taylor J.S., Raes J. Small-scale gene duplication. The Evolution of the Genome 2005, Elsevier Academic Press, London. T.R. Gregory (Ed.).
115. Taylor J.S., Braasch I., Frickey T., Meyer A., Van der Peer Y. Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res. 2003, 13:382-390.
116. Temple S.E., Veldhoen K.M., Phelan J.T., Veldhoen N.J., Hawryshyn C.W. Ontogenetic changes in photoreceptor opsin gene expression in coho salmon (Oncorhynchus kisutch, Walbaum). J. Exp. Biol. 2008, 211:3879-3888.
117. Tsujimura T., Chinen A., Kawamura S. Identification of a locus control region for quadruplicated green-sensitive opsin genes in zebrafish. Proc. Natl. Acad. Sci. USA 2007, 104:12813-12818.
118. Venkatesh B., Ning Y., Brenner S. Late changes in spliceosomal introns define clades in vertebrate evolution. Proc. Natl. Acad. Sci. USA 1999, 96:10267-10271.
119. Vihtelic T.S., Doro C.J., Hyde D.R. Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Visual Neurosci. 1999, 16:571-585.
120. Wagner H.J. Retinal structure of fishes. The Visual System of Fish 1990, 109-157. Chapman and Hall Ltd., London. M. Djamgoz (Ed.).
121. Wang D., Oakley T., Mower J., Shimmin L.C., Yim S., Honeycutt R.L., Tsao H., Li W.H. Molecular evolution of bat color vision genes. Mol. Biol. Evol. 2004, 21:295-302.
122. Ward M.N., Churcher A.M., Dick K.J., Laver C.R.J., Owens G.L., Polack M.D., Ward P.R., Breden F., Taylor J.S. The molecular basis of color vision in colorful fish: four Long Wave-Sensitive (LWS) opsins in guppies (Poecilia reticulata) are defined by amino acid substitutions at key functional sites. BMC Evol. Biol. 2008, 8:210.
123. Watson C.T., Lubieniecki K.P., Loew E., Davidson W.S., Breden F. Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. BMC Evol. Biol. 2010, 10:87.
124. Watson C.T., Gray S.M., Hoffmann M., Lubieniecki K.P., Joy J.B., Sandkam B.A., Weigel D., Loew E., Davidson W.S., Breden F. Gene duplication and divergence of long wavelength-sensitive opsin genes in the guppy, Poecilia reticulata. J. Mol. Evol. 2010, 72:240-252.
125. Weadick C.J., Chang B.S. Long-wavelength sensitive visual pigments of the guppy (Poecilia reticulata): six opsins expressed in a single individual. BMC Evol. Biol. 2007, 7:S11.
126. Winderickx J., Battisti L., Motulsky A.G., Deeb S.S. Selective expression of human X chromosome-linked green opsin genes. Proc. Natl. Acad. Sci. USA 1992, 89:9710-9714.
127. Winderickx J., Battisti L., Hibiya Y., Motulsky A.G., Deeb S.S. Haplotype diversity in the human red and green opsin genes: evidence for frequent sequence exchange in exon 3. Hum. Mol. Genet. 1993, 2:1413-1421.
128. Windsor D.J., Owens G.L. The opsin repertoire of Jenynsia onca: a new perspective on gene duplication and divergence in livebearers. BMC Res. Notes 2009, 2:159.
129. Wong W.S., Yang Z., Goldman N., Nielsen R. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 2004, 168:1041-1051.
130. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 2007, 24:1586-1591.
131. Yang Z., Nielsen R., Goldman N., Pedersen A.M. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
132. Yang Z., Wong W.S., Nielsen R. Bayes empirical bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 2005, 22:1107-1118.
133. Yokoyama S. Gene duplications and evolution of the short wavelength-sensitive visual pigments in vertebrates. Mol. Biol. Evol. 1994, 11:32-39.
134. Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog. Retin. Eye Res. 2000, 19:385-420.
135. Yokoyama S., Radlwimmer F.B. The " five-sites" rule and the evolution of red and green color vision in mammals. Mol. Biol. Evol. 1998, 15:560-567.
136. Yokoyama S., Tada T. Evolutionary dynamics of rhodopsin type 2 opsins in vertebrates. Mol. Biol. Evol. 2010, 27:133-141.
137. Yokoyama S., Tada T., Zhang H., Britt L. Elucidation of phenotypic adaptations: molecular analyses of dim-light vision proteins in vertebrates. Proc. Natl. Acad. Sci. USA 2008, 105:13480-13485.
138. Zhang J., Nielsen R., Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 2005, 22:2472-2479.