Journal of Molecular Evolution

, Volume 72, Issue 2, pp 240–252 | Cite as

Gene Duplication and Divergence of Long Wavelength-Sensitive Opsin Genes in the Guppy, Poecilia reticulata

  • Corey T. Watson
  • Suzanne M. Gray
  • Margarete Hoffmann
  • Krzysztof P. Lubieniecki
  • Jeffrey B. Joy
  • Ben A. Sandkam
  • Detlef Weigel
  • Ellis Loew
  • Christine Dreyer
  • William S. Davidson
  • Felix Breden


Female preference for male orange coloration in the genus Poecilia suggests a role for duplicated long wavelength-sensitive (LWS) opsin genes in facilitating behaviors related to mate choice in these species. Previous work has shown that LWS gene duplication in this genus has resulted in expansion of long wavelength visual capacity as determined by microspectrophotometry (MSP). However, the relationship between LWS genomic repertoires and expression of LWS retinal cone classes within a given species is unclear. Our previous study in the related species, Xiphophorus helleri, was the first characterization of the complete LWS opsin genomic repertoire in conjunction with MSP expression data in the family Poeciliidae, and revealed the presence of four LWS loci and two distinct LWS cone classes. In this study we characterized the genomic organization of LWS opsin genes by BAC clone sequencing, and described the full range of cone cell types in the retina of the colorful Cumaná guppy, Poecilia reticulata. In contrast to X. helleri, MSP data from the Cumaná guppy revealed three LWS cone classes. Comparisons of LWS genomic organization described here for Cumaná to that of X. helleri indicate that gene divergence and not duplication was responsible for the evolution of a novel LWS haplotype in the Cumaná guppy. This lineage-specific divergence is likely responsible for a third additional retinal cone class not present in X. helleri, and may have facilitated the strong sexual selection driven by female preference for orange color patterns associated with the genus Poecilia.


Opsin Gene duplication Sexual selection Gene conversion 

Supplementary material

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Supplementary material 1 (XLS 24 kb)
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Supplementary material 2 (PDF 295 kb)
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Supplementary material 3 (PDF 553 kb)
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Supplementary material 4 (DOC 48 kb)


  1. Alexander HJ, Breden F (2004) Sexual isolation and extreme morphological divergence in the Cumaná guppy: a possible case of incipient speciation. J Evol Biol 17:1238–1254PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Archer SN, Lythgoe JN (1990) The visual pigment basis for cone polymorphism in the guppy, Poecilia reticulata. Vis Res 30:225–233PubMedCrossRefGoogle Scholar
  4. Archer SN, Endler JA, Lythgoe JN, Partridge JC (1987) Visual pigment polymorphism in the guppy, Poecilia reticulata. Vis Res 27:1243–1252PubMedCrossRefGoogle Scholar
  5. Bourne GR, Breden F, Allen TC (2003) Females prefer carotenoid colored males as mates in the pentamorphic livebearing fish, Poecilia parae. Naturwissenschaften 90:402–405PubMedCrossRefGoogle Scholar
  6. Bowmaker J, Loew E (2008) Vision in fish. In: Masland R, Albright T (eds) The senses: a comprehensive reference. Elsevier, Boston, pp 53–76CrossRefGoogle Scholar
  7. Breden F, Stoner G (1987) Male predation risk determines female preference in the Trinidad guppy. Nature 329:831–833CrossRefGoogle Scholar
  8. Carleton KL (2009) Cichlid fish visual systems: mechanisms of spectral tuning. Integr Zool 4:75–86PubMedCrossRefGoogle Scholar
  9. Chinen A, Hamaoka T, Yamada Y, Kawamura S (2003) Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–675PubMedGoogle Scholar
  10. Endler JA (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fishes 9:173–190CrossRefGoogle Scholar
  11. Endler JA, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468CrossRefGoogle Scholar
  12. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194PubMedGoogle Scholar
  13. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185PubMedGoogle Scholar
  14. 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 190:147–154CrossRefGoogle Scholar
  15. Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202PubMedGoogle Scholar
  16. Hoffmann M, Tripathi N, Henz SR, Lindholm AK, Weigel D, Breden F, Dreyer C (2007) Opsin gene duplication and diversification in the guppy, a model for sexual selection. Proc R Soc B 274:33–42PubMedCrossRefGoogle Scholar
  17. Hofmann CM, Carleton KL (2009) Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish. J Int Comp Biol 49:630–643CrossRefGoogle Scholar
  18. Houde AE (1987) Mate choice based upon naturally-occurring color-pattern variation in a guppy population. Evolution 41:1–10CrossRefGoogle Scholar
  19. Houde AE, Endler JA (1990) Correlated evolution of female mating preferences and male color patterns in the Guppy Poecilia reticulata. Science 248:1405–1408PubMedCrossRefGoogle Scholar
  20. Hubbard TJP, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, Brent S, Chen Y, Clapham P, Clarke L, Coates G, Fairley S, Fitzgerald S, Fernandez-Banet J, Gordon L, Graf S, Haider S, Hammond M, Holland R, Howe K, Jenkinson A, Johnson N, Kahari A, Keefe D, Keenan S, Kinsella R, Kokocinski F, Kulesha E, Lawson D, Longden I, Megy K, Meidl P, Overduin B, Parker A, Pritchard B, Rios D, Schuster M, Slater G, Smedley D, Spooner W, Spudich G, Trevanion S, Vilella A, Vogel J, White S, Wilder S, Zadissa A, Birney E, Cunningham F, Curwen V, Durbin R, Fernandez-Suarez XM, Herrero J, Kasprzyk A, Proctor G, Smith J, Searle S, Flicek P (2009) Ensembl 2009. Nucl Acids Res 37:D690–D697PubMedCrossRefGoogle Scholar
  21. Johnstone KA, Lubieniecki KP, Chow W, Phillips RB, Koop BF, Davidson WS (2008) Genomic organization and characterization of two vomeronasal 1 receptor-like genes (ora1 and ora2) in Atlantic salmon Salmo salar. Mar Genomics 1:23–31CrossRefGoogle Scholar
  22. Kathoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64CrossRefGoogle Scholar
  23. Kawamura S, Blow NS, Yokoyama S (1999) Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics 153:1839–1850PubMedGoogle Scholar
  24. Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664PubMedGoogle Scholar
  25. Kodric-Brown A (1985) Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 17:199–205CrossRefGoogle Scholar
  26. Körner KE, Schlupp I, Plath M, Loew ER (2006) Spectral sensitivity of mollies: comparing surface- and cave-dwelling Atlantic mollies, Poecilia mexicana. J Fish Biol 69:54–65CrossRefGoogle Scholar
  27. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580PubMedCrossRefGoogle Scholar
  28. Lindholm AK, Brooks R, Breden F (2004) Extreme polymorphism in a Y-linked sexually selected trait. Heredity 92:156–162PubMedCrossRefGoogle Scholar
  29. Lipetz LE, Cronin TW (1988) Application of an invariant spectral form to the visual pigments of crustaceans: implications regarding the binding of the chromophore. Vis Res 28:1083–1093PubMedCrossRefGoogle Scholar
  30. Loew ER (1994) A third, ultraviolet-sensitive, visual pigment in the Tokay Gecko (Gecko gekko). Vis Res 34:1427–1431PubMedCrossRefGoogle Scholar
  31. MacNichol EF (1986) A unifying presentation of photopigment spectra. Vis Res 26:1543–1556PubMedCrossRefGoogle Scholar
  32. Mansai SP, Innan H (2010) The power of the methods for detecting interlocus gene conversion. Genetics 184:517–527PubMedCrossRefGoogle Scholar
  33. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Tasneem A, Thanki N, Yamashita RA, Zhang D, Zhang N, Bryant SH (2009) CDD: specific functional annotation with the conserved domain database. Nucl Acids Res 37:D205–D210PubMedCrossRefGoogle Scholar
  34. Matsumoto Y, Fukamach S, Mitam H, Kawamura S (2006) Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371:268–278PubMedCrossRefGoogle Scholar
  35. Meredith RW, Pires MN, Reznick DN, Springer MS (2010) Molecular phylogenetic relationships and the evolution of the placenta in Poecilia (Micropoecilia) (Poeciliidae: Cyprinodontiformes). Mol Phylogenet Evol 55:631–639PubMedCrossRefGoogle Scholar
  36. Neafsey DE, Hartl DL (2005) Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon pufferfish lineages. Gene 350:161–171PubMedCrossRefGoogle Scholar
  37. Ning ZM, Cox AJ, Mullikin JC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11:1725–1729PubMedCrossRefGoogle Scholar
  38. Nylander JA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, SwedenGoogle Scholar
  39. Nylander JA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583PubMedCrossRefGoogle Scholar
  40. Owens GL, Windsor DJ, Mui J, Taylor JS (2009) A fish eye out of water: ten visual opsins in the four-eyed fish, Anableps anableps. PLoS One 4:e5970PubMedCrossRefGoogle Scholar
  41. Press W, Flannery B, Teukolsky S, Vetterling W (1987) Numerical recipes in Pascal. Cambridge University Press, CambridgeGoogle Scholar
  42. Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucl Acids Res 35:D61–D65PubMedCrossRefGoogle Scholar
  43. Rambaut A (1996) Se-Al: sequence alignment editor.
  44. Rambaut A, Drummond AJ (2007) Tracer v1.4.
  45. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  46. Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9PubMedCrossRefGoogle Scholar
  47. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116Google Scholar
  48. Smallwood PM, Wang Y, Nathans J (2002) Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proc Natl Acad Sci USA 99:1008–1011PubMedCrossRefGoogle Scholar
  49. Spady TC, Parry JW, Robinson PR, Hunt DM, Bowmaker JK, Carleton KL (2006) Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Mol Biol Evol 23:1538–1547PubMedCrossRefGoogle Scholar
  50. Suzek BE, Huang HZ, McGarvey P, Mazumder R, Wu CH (2007) UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23:1282–1288PubMedCrossRefGoogle Scholar
  51. Swofford DL (2003) PAUP*. Phylogenetic analysis using Parsimony (*and Other Methods), version 4. Sinauer Associates, SunderlandGoogle Scholar
  52. Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244CrossRefGoogle Scholar
  53. Tripathi N, Hoffmann M, Willing EM, Lanz C, Weigel D, Dreyer C (2009a) Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation. Proc R Soc B 276:2195–2208PubMedCrossRefGoogle Scholar
  54. Tripathi N, Hoffmann M, Weigel D, Dreyer C (2009b) Linkage analysis reveals the independent origin of Poeciliid sex chromosomes and a case of atypical sex inheritance in the Guppy (Poecilia reticulata). Genetics 182:365–374PubMedCrossRefGoogle Scholar
  55. Tsujimura T, Chinen A, Kawamura S (2007) Identification of a locus control region for quadruplicated green-sensitive opsin genes in zebrafish. Proc Natl Acad Sci USA 104:12813–12818PubMedCrossRefGoogle Scholar
  56. Wakefield MJ, Anderson M, Chang E, Wei KJ, Kaul R, Graves JAM, Grutzner F, Deeb SS (2008) Cone visual pigments of monotremes: filling the phylogenetic gap. Vis Neurosci 25:257–264PubMedCrossRefGoogle Scholar
  57. Wang Y, Macke JP, Merbs SL, Zack DJ, Klaunberg B, Bennett J, Gearhart J, Nathans J (1992) A locus control region adjacent to the human red and green visual pigment genes. Neuron 9:429–440PubMedCrossRefGoogle Scholar
  58. Ward MN, Churcher AM, Dick KJ, Laver CRJ, Owens GL, Polack MD, Ward PR, Breden F, Taylor JS (2008) 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 8:210PubMedCrossRefGoogle Scholar
  59. Watson CT, Lubieniecki KP, Loew E, Davidson WS, Breden F (2010) Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. BMC Evol Biol 10:87PubMedCrossRefGoogle Scholar
  60. Weadick CJ, Chang BSW (2007) Long-wavelength sensitive visual pigments of the guppy (Poecilia reticulata): six opsins expressed in a single individual. BMC Evol Biol 7(Suppl 1):S11PubMedCrossRefGoogle Scholar
  61. Willing EM, Bentzen P, van Oosterhout C, Hoffmann M, Cable J, Breden F, Weigel D, Dreyer C (2010) Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Mol Ecol 19:968–984PubMedCrossRefGoogle Scholar
  62. Windsor DJ, Owens GL (2009) The opsin repertoire of Jenynsia onca: a new perspective on gene duplication and divergence in livebearers. BMC Res Notes 2:159PubMedCrossRefGoogle Scholar
  63. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419PubMedCrossRefGoogle Scholar
  64. Yokoyama S, Radlwimmer B (1998) The “five-sites” rule and the evolution of red and green color vision in mammals. Mol Biol Evol 15:560–567PubMedGoogle Scholar
  65. Yokoyama S, Radlwimmer FB (2001) The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158:1697–1710PubMedGoogle Scholar
  66. Yokoyama R, Yokoyama S (1990) Convergent evolution of the red-like and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc Nat Acad Sci USA 87:9315–9318PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Corey T. Watson
    • 1
  • Suzanne M. Gray
    • 2
  • Margarete Hoffmann
    • 3
  • Krzysztof P. Lubieniecki
    • 4
  • Jeffrey B. Joy
    • 1
  • Ben A. Sandkam
    • 1
  • Detlef Weigel
    • 3
  • Ellis Loew
    • 5
  • Christine Dreyer
    • 3
  • William S. Davidson
    • 4
  • Felix Breden
    • 1
  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  2. 2.Department of BiologyMcGill UniversityMontrealCanada
  3. 3.Department of Molecular BiologyMax Planck Institute for Developmental BiologyTuebingenGermany
  4. 4.Department of Molecular Biology and BiochemistrySimon Fraser UniversityBurnabyCanada
  5. 5.Department of Biomedical SciencesCornell UniversityIthacaUSA

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