Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays

Molecular Biology and Evolution

Volumn 23, Issue 8, 2006, Pages 1538-1547

  Spady, Tyrone C ^a,d   Parry, Juliet W L ^b   Robinson, Phyllis R ^c   Hunt, David M ^b   Bowmaker, James K ^b   Carleton, Karen L ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Cichlid; Gene expression; Opsin; Real time RT PCR; Subfunctionalization; Visual pigment

Indexed keywords

MESSENGER RNA; OPSIN; VISUAL PIGMENT;

ADAPTIVE RADIATION; ARTICLE; CICHLID; CONTROLLED STUDY; EMBRYO; FISH GENETICS; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC SELECTION; HUMAN; HUMAN CELL; LAKE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; OREOCHROMIS NILOTICUS; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECTRAL SENSITIVITY; TILAPIA;

ANIMALS; CELL LINE; CICHLIDS; CONES (RETINA); EVOLUTION, MOLECULAR; FISHES; HUMANS; MOLECULAR SEQUENCE DATA; OPSIN; PHYLOGENY; RETINAL CONE PHOTORECEPTOR CELLS; ROD OPSINS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SPECTRUM ANALYSIS; TRANSFECTION;

AFRICAN CICHLIDS; CICHLIDAE; OREOCHROMIS NILOTICUS; PISCES; TILAPIA;

EID: 33748072399     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl014     Document Type: Article

References (64)

1. Asenjo AB, Rim J, Oprian DD. 1994. Molecular determinants of human red/green color discrimination. Neuron 12:1131-8.
2. Ban E, Kasai A, Sato M, Yokozeki A, Hisatomi O, Oshima N. 2005. The signaling pathway in photoresponses that may be mediated by visual pigments in erythrophores of Nile tilapia. Pigment Cell Res 18:360-9.
3. Briscoe AD. 2001. Functional diversification of lepidopteran opsins following gene duplication. Mol Biol Evol 18:2270-9.
4. Carleton KL, Harosi FI, Kocher TD. 2000. Visual pigments of African cichlid fishes: evidence for ultraviolet vision from microspectrophotometry and DNA sequences. Vision Res 40:879-90.
5. Carleton KL, Kocher TD. 2001. Cone opsin genes of african cichlid fishes: tuning spectral sensitivity by differential gene expression. Mol Biol Evol 18:1540-50.
6. Carleton KL, Parry JWL, Bowmaker JK, Hunt DM, Seehausen O. 2005. Color vision and speciation in Lake Victoria cichlids of the genus Pundamilia. Mol Ecol 14:4341-53.
7. Carleton KL, Spady TC, Kocher TD. 2006. Visual communication in East African cichlid fishes: diversity in a phylogenetic context. In: Ladich F, Collin SP, Moller P, Kapoor BG, editors. Communication in fishes. Enfield, NH: Science Publisher Inc. p 481-511.
8. Chang BS, Crandall KA, Carulli JP, Hartl DL. 1995. Opsin phylogeny and evolution: a model for blue shifts in wavelength regulation. Mol Phylogenet Evol 4:31-43.
9. Chen WJ, Orti G, Meyer A. 2004. Novel evolutionary relationship among four fish model systems. Trends Genet 20:424-31.
10. Chinen A, Hamaoka T, Yamada Y, Kawamura S. 2003. Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663-75.
11. Collin SP, Knight MA, Davies WL, Potter IC, Hunt DM, Trezise AE. 2003. Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864-5.
12. Cowing JA, Poopalasundaram S, Wilkie SE, Bowmaker JK, Hunt DM. 2002. Spectral tuning and evolution of short wave-sensitive cone pigments in cottoid fish from Lake Baikal. Biochemistry 41:6019-25.
13. Cowing JA, Poopalasundaram S, Wilkie SE, Robinson PR, Bowmaker JK, Hunt DM. 2002. The molecular mechanism for the spectral shifts between vertebrate ultraviolet- and violet-sensitive cone visual pigments. Biochem J 367:129-35.
14. Deutschlander ME, Greaves DK, Haimberger TJ, Hawryshyn CW. 2001. Functional mapping of ultraviolet photosensitivity during metamorphic transitions in a salmonid fish, Oncorhynchus mykiss. J Exp Biol 204:2401-13.
15. Dulai KS, von Dornum M, Mollon JD, Hunt DM. 1999. The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res 9:629-38.
16. Fernald RD, Liebman PA. 1980. Visual receptor pigments in the African cichlid fish, Haplochromis burtoni. Vision Res 20:857-64.
17. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-45.
18. Forsell J, Ekstrom P, Flamarique IN, Holmqvist B. 2001. Expression of pineal ultraviolet- and green-like opsins in the pineal organ and retina of teleosts. J Exp Biol 204:2517-25.
19. Forsell J, Holmqvist B, Ekstrom P. 2002. Molecular identification and developmental expression of UV and green opsin mRNAs in the pineal organ of the Atlantic halibut. Brain Res Dev Brain Res 136:51-62.
20. Francino MP. 2005. An adaptive radiation model for the origin of new gene functions. Nat Genet 37:573-7.
21. Franke RR, Sakmar TP, Oprian DD, Khorana HG. 1988. A single amino acid substitution in rhodopsin (lysine 248 - leucine) prevents activation of transducin. J Biol Chem 263:2119-22.
22. Fuller RC, Carleton KL, Fadool JM, Spady TC, Travis J. 2004. Population variation in opsin expression in the bluefin killifish, Lucania goodei: a real-time PCR study. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:147-54.
23. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K. 2000. In search of the visual pigment template. Vis Neurosci 17:509-28.
24. Halstenberg S, Lindgren KM, Samagh SP, Nadal-Vicens M, Balt S, Fernald RD. 2005. Diurnal rhythm of cone opsin expression in the teleost fish Haplochromis burtoni. Vis Neurosci 22:135-41.
25. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ. 2002. G protein-coupled receptors in Anopheles gambiae. Science 298:176-8.
26. Hisatomi O, Kayada S, Aoki Y, Iwasa T, Tokunaga F. 1994. Phylogenetic relationships among vertebrate visual pigments. Vision Res 34:3097-102.
27. Hunt DM, Cowing JA, Wilkie SE, Parry JW, Poopalasundaram S, Bowmaker JK. 2004. Divergent mechanisms for the tuning of shortwave sensitive visual pigments in vertebrates. Photochem Photobiol Sci 3:713-20.
28. Ibbotson RE, Hunt DM, Bowmaker JK, Mollon JD. 1992. Sequence divergence and copy number of the middle- and long-wave photopigment genes in Old World monkeys. Proc Biol Sci 247:145-54.
29. Jacobs GH, Neitz M, Deegan JF, Neitz J. 1996. Trichromatic colour vision in New World monkeys. Nature 382:156-8.
30. Johnson RL, Grant KB, Zankel TC, Boehm MF, Merbs SL, Nathans J, Nakanishi K. 1993. Cloning and expression of goldfish opsin sequences. Biochemistry 32:208-14.
31. Jordan RC, Kellogg KA, Juanes JR, Loew ER. 2006. Photopigment sensitivities across taxa of Lake Malawi cichlids. J Fish Biol 68:1291-9.
32. Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF. 1995. Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Mol Phylogenet Evol 4:420-32.
33. Kumazawa Y, Yamaguchi M, Nishida M. 1999. Mitochondrial molecular clocks and the origin of euteleostean biodiversity: familial radiation of perciforms may have predated the cretaceous/tertiary boundary. In: Kato M, editor. The biology of biodiversity. Tokyo, Japan: Springer-Verlag. p 35-52.
34. Levine JS, MacNichol EF Jr. 1979. Visual pigments in teleost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. Sens Processes 3:95-131.
35. Lynch M. 2002. Genomics. Gene duplication and evolution. Science 297:945-7.
36. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-5.
37. Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302:1401-4.
38. Mader MM, Cameron DA. 2004. Photoreceptor differentiation during retinal development, growth, and regeneration in a metamorphic vertebrate. J Neurosci 24:11463-72.
39. Matsumoto Y, Fukamachi S, Mitani H, Kawamura S. 2006. Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371:268-78.
40. Minamoto T, Shimizu I. 2005. Molecular cloning of cone opsin genes and their expression in the retina of a smelt, Ayu (Plecoglossus altivelis, Teleostei). Comp Biochem Physiol B Biochem Mol Biol 140:197-205.
41. Miya M, Takeshima H, Endo H, et al. (12 co-authors). 2003. Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121-38.
42. Molday RS, MacKenzie D. 1983. Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry 22:653-60.
43. Nathans J, Thomas D, Hogness DS. 1986. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232:193-202.
44. Neafsey DE, Hartl DL. 2005. Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon puffer fish lineages. Gene 350:161-71.
45. Nelson JS. 1994. Fishes of the world. New York: John Wiley & Sons, Inc.
46. Ohno S. 1970. Evolution by gene duplication. New York: Springer Verlag.
47. Oprian DD, Molday RS, Kaufman RJ, Khorana HG. 1987. Expression of a synthetic bovine rhodopsin gene in monkey kidney cells. Proc Natl Acad Sci USA 84:8874-8.
48. Palczewski K, Kumasaka T, Hori T, et al. (12 co-authors). 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739-45.
49. Parry JWL, Carleton KL, Spady T, Carboo A, Hunt DM, Bowmaker JK. 2005. Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in lake Malawi cichlids. Curr Biol 15:1734-9.
50. 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 43:8014-20.
51. Rastogi S, Liberles DA. 2005. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol Biol 5:28.
52. Register EA, Yokoyama R, Yokoyama S. 1994. Multiple origins of the green-sensitive opsin genes in fish. J Mol Evol 39:268-73.
53. Saitoh K, Miya M, Inoue JG, Ishiguro NB, Nishida M. 2003. Mitochondrial genomics of ostariophysan fishes: perspectives on phylogeny and biogeography. J Mol Evol 56:464-72.
54. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-25.
55. Spady TC, Seehausen O, Loew ER, Jordan RC, Kocher TD, Carleton KL. 2005. Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species. Mol Biol Evol 22:1412-22.
56. Spaethe J, Briscoe AD. 2004. Early duplication and functional diversification of the opsin gene family in insects. Mol Biol Evol 21:1583-94.
57. Swofford, DL. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, MA: Sinauer Associates.
58. Takahashi Y, Ebrey TG. 2003. Molecular basis of spectral tuning in the newt short wavelength sensitive visual pigment. Biochemistry 42:6025-34.
59. Takechi M, Kawamura S. 2005. Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. J Exp Biol 208:1337-45.
60. Trezise AE, Collin SP. 2005. Opsins: evolution in waiting. Curr Biol 15:R794-6.
61. Wilkie SE, Robinson PR, Cronin TW, Poopalasundaram S, Bowmaker JK, Hunt DM. 2000. Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments. Biochemistry 39:7895-901.
62. Yokoyama R, Yokoyama S. 1990. Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc Natl Acad Sci USA 87:9315-8.
63. Yokoyama S. 1994. Gene duplications and evolution of the short wavelength-sensitive visual pigments in vertebrates. Mol Biol Evol 11:32-9.
64. Yokoyama S, Blow NS, Radlwimmer FB. 2000. Molecular evolution of color vision of zebra finch. Gene 259:17-24.