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Distinct Evolutionary Patterns Between Two Duplicated Color Vision Genes Within Cyprinid Fishes

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Abstract

We investigated the molecular evolution of duplicated color vision genes (LWS-1 and SWS2) within cyprinid fish, focusing on the most cavefish-rich genus—Sinocyclocheilus. Maximum likelihood-based codon substitution approaches were used to analyze the evolution of vision genes. We found that the duplicated color vision genes had unequal evolutionary rates, which may lead to a related function divergence. Divergence of LWS-1 was strongly influenced by positive selection causing an accelerated rate of substitution in the proportion of pocket-forming residues. The SWS2 pigment experienced divergent selection between lineages, and no positively selected site was found. A duplicate copy of LWS-1 of some cyprinine species had become a pseudogene, but all SWS2 sequences remained intact in the regions examined in the cyprinid fishes examined in this study. The pseudogenization events did not occur randomly in the two copies of LWS-1 within Sinocyclocheilus species. Some cave species of Sinocyclocheilus with numerous morphological specializations that seem to be highly adapted for caves, retain both intact copies of color vision genes in their genome. We found some novel amino acid substitutions at key sites, which might represent interesting target sites for future mutagenesis experiments. Our data add to the increasing evidence that duplicate genes experience lower selective constraints and in some cases positive selection following gene duplication. Some of these observations are unexpected and may provide insights into the effect of caves on the evolution of color vision genes in fishes.

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References

  • Betrán E, Long M (2003) Dntf-2r, a young Drosophila retroposed gene with specific male expression under positive Darwinian selection. Genetics 164:977–988

    PubMed  Google Scholar 

  • Bielawski JP, Yang Z (2001) Positive and negative selection in the DAZ gene family. Mol Biol Evol 18:523–529

    CAS  PubMed  Google Scholar 

  • Bielawski JP, Yang Z (2004) A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J Mol Evol 59:121–132

    Article  CAS  PubMed  Google Scholar 

  • Bowmaker JK (1995) The visual pigments of fish. Prog Retin Eye Res 15:1–31

    Article  Google Scholar 

  • Charlat S, Hornett EA, Fullard JH, Davies N, Roderick GK, Wedell N, Hurst GD (2007) Extraordinary flux in sex ratio. Science 317:214

    Article  CAS  PubMed  Google Scholar 

  • Chinen A, Hamaoka T, Yamada Y, Kawamura S (2003) Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–675

    CAS  PubMed  Google Scholar 

  • Crandall KA, Hillis DM (1997) Rhodopsin evolution in the dark. Nature 387:667–668

    Article  CAS  PubMed  Google Scholar 

  • Crescitelli F (1972) The visual cells and visual pigments of the vertebrate eye. In: Dartnall HJA (ed) Handbook of sensory physiology, vol VII/1. Springer-Verlag, Berlin, pp 245–363

    Google Scholar 

  • Crow KD, Stadler PF, Lynch VJ, Amemiya C, Wagner GP (2006) The “fish-specific” Hox cluster duplication is coincident with the origin of teleosts. Mol Biol Evol 23:121–136

    Article  CAS  PubMed  Google Scholar 

  • Fares MA, Wolfe KH (2003) Positive selection and subfunctionalization of duplicated CCT chaperonin subunits. Mol Biol Evol 20:1588–1597

    Article  CAS  PubMed  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    CAS  PubMed  Google Scholar 

  • Hoegg S, Brinkmann H, Taylor JS, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203

    Article  CAS  PubMed  Google Scholar 

  • Honig B, Greenberg AD, Dinur U, Ebrey TG (1976) Visual-pigment spectra: implications of the protonation of the retinal Schiff base. Biochemistry 15:4593–4599

    Article  CAS  PubMed  Google Scholar 

  • Hunt DM, Fitzgibbon J, Slobodyanyuk SJ, Bowmaker JK (1996) Spectral tuning and molecular evolution of rod visual pigments in the species flock of cottoid fish in Lake Baikal. Vision Res 36:1217–1224

    Article  CAS  PubMed  Google Scholar 

  • Kito Y, Suzuki T, Azuma M, Sekoguti Y (1968) Absorption spectrum of rhodopsin denatured with acid. Nature 218:955–957

    Article  CAS  PubMed  Google Scholar 

  • Kochendoerfer GG, Lin SW, Sakmar TP, Mathies RA (1999) How color visual pigments are tuned. Trends Biochem Sci 24:300–305

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Li Z, He S (2009) Relaxed purifying selection of rhodopsin gene within a Chinese endemic cavefish genus Sinocyclocheilus (Pisces: Cypriniformes). Hydrobiologia 624:139–149

    Article  CAS  Google Scholar 

  • Li J, Wang X, Kong X, Zhao K, He S, Mayden RL (2008a) Variation patterns of the mitochondrial 16S rRNA gene with secondary structure constraints and their application to phylogeny of cyprinine fishes (Teleostei: Cypriniformes). Mol Phylogenet Evol 47:472–487

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Guo B, Li J, He S, Chen Y (2008b) Bayesian mixed models and divergence time estimation of Chinese cavefishes (Cyprinidae: Sinocyclocheilus). Chin Sci Bull 53:2342–2352

    Article  CAS  Google Scholar 

  • Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473

    CAS  PubMed  Google Scholar 

  • Málaga-Trillo E, Laessing U, Lang DM, Meyer A, Stuermer CA (2002) Evolution of duplicated reggie genes in zebrafish and goldfish. J Mol Evol 54:235–245

    Article  PubMed  Google Scholar 

  • Maston GA, Ruvolo M (2002) Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection. Mol Biol Evol 19:320–335

    CAS  PubMed  Google Scholar 

  • Mathews S, Burleigh JG, Donoghue MJ (2003) Adaptive evolution in the photosensory domain of phytochrome A in early angiosperms. Mol Biol Evol 20:1087–1097

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Zhang J, Yokoyama S (1997) Color vision of ancestral organisms of higher primates. Mol Biol Evol 14:611–618

    CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York

    Google Scholar 

  • Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–745

    Article  CAS  PubMed  Google Scholar 

  • Perry GH, Martin RD, Verrelli BC (2007) Signatures of functional constraint at aye-aye opsin genes: the potential of adaptive color vision in a nocturnal primate. Mol Biol Evol 24:1963–1970

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38:107–111

    Article  CAS  PubMed  Google Scholar 

  • Rasquin P (1949) The influence of light and darkness on thyroid and pituitary activity of the characin, Astyanax mexicanus and its cave derivates. Bull Am Mus Nat Hist 93:497–532

    Google Scholar 

  • Rasquin P, Rosenbloom L (1954) Endocrine imbalance and tissue hyperplasia in teleostes maintained in darkness. Bull Am Mus Nat Hist 104:357–426

    Google Scholar 

  • Rodriguez-Trelles F, Tarrio R, Ayala FJ (2003) Convergent neofunctionalization by positive Darwinian selection after ancient recurrent duplications of the xanthine dehydrogenase gene. Proc Natl Acad Sci USA 100:13413–13417

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HD, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–626

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Yokoyama S (2003) Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 100:8308–8313

    Article  CAS  PubMed  Google Scholar 

  • 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 22:1412–1422

    Article  CAS  PubMed  Google Scholar 

  • Sugawara T, Terai Y, Okada N (2002) Natural selection of the rhodopsin gene during the adaptive radiation of East African Great Lakes cichlid fishes. Mol Biol Evol 19:1807–1811

    CAS  PubMed  Google Scholar 

  • Tan Y, Yoder AD, Yamashita N, Li WH (2005) Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci USA 102:14712–14716

    Article  CAS  PubMed  Google Scholar 

  • Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13:382–390

    Article  CAS  PubMed  Google Scholar 

  • Terai Y, Seehausen O, Sasaki T, Takahashi K, Mizoiri S, Sugawara T, Sato T, Watanabe M, Konijnendijk N, Mrosso HD, Tachida H, Imai H, Shichida Y, Okada N (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biol 4:e433

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequences alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Walls GL (1934) The reptilian retina. Am J Ophthalmol 17:892–915

    Google Scholar 

  • Walsh JB (1995) How often do duplicated genes evolve new functions? Genetics 139:421–428

    CAS  PubMed  Google Scholar 

  • Wang FY, Chung WS, Yan HY, Tzeng CS (2008) Adaptive evolution of cone opsin genes in two colorful cyprinids, Opsariichthys pachycephalus and Candidia barbatus. Vision Res 48:1695–1704

    Article  CAS  PubMed  Google Scholar 

  • Xiao H, Zhang RD, Feng JG, Ou Y, Li W, Chen S, Zan R (2002) Nuclear DNA content and ploidy of seventeen species of fishes in Sinocyclocheilus. Zool Res 23:195–199

    CAS  Google Scholar 

  • Xiao H, Chen S, Liu Z, Zhang R, Li W, Zan R, Zhang Y (2005) Molecular phylogeny of Sinocyclocheilus (Cypriniformes: Cyprinidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 36:67–77

    Article  CAS  PubMed  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    CAS  PubMed  Google Scholar 

  • Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15:568–573

    CAS  PubMed  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    CAS  PubMed  Google Scholar 

  • Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S (2002) Molecular evolution of color vision in vertebrates. Gene 300:69–78

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S (2008) Evolution of dim-light and color vision pigments. Annu Rev Genomics Hum Genet 9:259–282

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S, Radlwimmer FB (2001) The molecular genetics of red and green color vision in vertebrates. Genetics 158:1697–1710

    CAS  PubMed  Google Scholar 

  • Yokoyama S, Tada T (2000) Adaptive evolution of the African and Indonesian coelacanths to deep-sea environments. Gene 261:35–42

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S, Takenaka N (2004) The molecular basis of adaptive evolution of squirrelfish rhodopsins. Mol Biol Evol 21:2071–2078

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S, Meany A, Wilkens H, Yokoyama R (1995) Initial mutational steps toward loss of opsin gene function in cavefish. Mol Biol Evol 12:527–532

    CAS  PubMed  Google Scholar 

  • Yokoyama S, Takenaka N, Blow N (2007) A novel spectral tuning in the short wavelength-sensitive (SWS1 and SWS2) pigments of bluefin killifish (Lucania goodei). Gene 396:196–202

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S, Tada T, Zhang H, Britt L (2008) Elucidation of phenotypic adaptations: molecular analyses of dim-light vision proteins in vertebrates. Proc Natl Acad Sci USA 105:13480–13485

    Article  CAS  PubMed  Google Scholar 

  • Yu XJ, Zhou T, Li YC, Li K, Zhou M (1989) Chromosomes of Chinese fresh-water fishes (in Chinese). Science Press, Beijing

    Google Scholar 

  • Yue PQ, Chen YY (1998) China red data book of endangered animals: Pisces. Science Press, Beijing

    Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

  • Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95:3708–3713

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang Y, Rosenberg HF (2002) Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet 30:411–415

    Article  CAS  PubMed  Google Scholar 

  • Zhao YH (2006) An endemic cavefish genus Sinocyclocheilus in China—species diversity, systematics, and zoogeography (Cypriniformes: Cyprinidae). PhD thesis, Institute of Zoology, Chinese Academy of Sciences, Beijing

  • Zhao Y, Zhang C (2006) Cavefishes: concept, diversity and research progress. Biodivers Sci 14:451–460

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank the members of He’s lab for their assistance. Zuogang Peng and Simon Y. W. Ho are gratefully acknowledged for critically reading this manuscript. We sincerely thank the two anonymous referees and the Associate Editor for their insightful comments on the earlier versions of this manuscript. This research has been supported by the grants from National Natural Science Foundation of China (NSFC) 2007CB411600 and 30530120 to S. H.

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Authors and Affiliations

  1. Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, 7th Donghu South Road, 430072, Wuhan, Hubei Province, People’s Republic of China

    Zhiqiang Li, Xiaoni Gan & Shunping He

  2. Graduate School of Chinese Academy of Sciences, Beijing, 100039, People’s Republic of China

    Zhiqiang Li & Xiaoni Gan

  3. Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, 430071, Hubei Province, People’s Republic of China

    Xiaoni Gan

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  1. Zhiqiang Li
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Correspondence to Shunping He.

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Li, Z., Gan, X. & He, S. Distinct Evolutionary Patterns Between Two Duplicated Color Vision Genes Within Cyprinid Fishes. J Mol Evol 69, 346–359 (2009). https://doi.org/10.1007/s00239-009-9283-9

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