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

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Abstract

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.

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References

  • Alexander HJ, Breden F (2004) Sexual isolation and extreme morphological divergence in the Cumaná guppy: a possible case of incipient speciation. J Evol Biol 17:1238–1254

    Article  PubMed  CAS  Google Scholar 

  • 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 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Archer SN, Lythgoe JN (1990) The visual pigment basis for cone polymorphism in the guppy, Poecilia reticulata. Vis Res 30:225–233

    Article  PubMed  CAS  Google Scholar 

  • Archer SN, Endler JA, Lythgoe JN, Partridge JC (1987) Visual pigment polymorphism in the guppy, Poecilia reticulata. Vis Res 27:1243–1252

    Article  PubMed  CAS  Google Scholar 

  • Bourne GR, Breden F, Allen TC (2003) Females prefer carotenoid colored males as mates in the pentamorphic livebearing fish, Poecilia parae. Naturwissenschaften 90:402–405

    Article  PubMed  CAS  Google Scholar 

  • Bowmaker J, Loew E (2008) Vision in fish. In: Masland R, Albright T (eds) The senses: a comprehensive reference. Elsevier, Boston, pp 53–76

    Chapter  Google Scholar 

  • Breden F, Stoner G (1987) Male predation risk determines female preference in the Trinidad guppy. Nature 329:831–833

    Article  Google Scholar 

  • Carleton KL (2009) Cichlid fish visual systems: mechanisms of spectral tuning. Integr Zool 4:75–86

    Article  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

    PubMed  CAS  Google Scholar 

  • Endler JA (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fishes 9:173–190

    Article  Google Scholar 

  • Endler JA, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468

    Article  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • 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 190:147–154

    Article  CAS  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • 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 274:33–42

    Article  PubMed  CAS  Google Scholar 

  • 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 49:630–643

    Article  CAS  Google Scholar 

  • Houde AE (1987) Mate choice based upon naturally-occurring color-pattern variation in a guppy population. Evolution 41:1–10

    Article  Google Scholar 

  • Houde AE, Endler JA (1990) Correlated evolution of female mating preferences and male color patterns in the Guppy Poecilia reticulata. Science 248:1405–1408

    Article  PubMed  CAS  Google Scholar 

  • 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–D697

    Article  PubMed  CAS  Google Scholar 

  • 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 1:23–31

    Article  Google Scholar 

  • Kathoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64

    Article  Google Scholar 

  • Kawamura S, Blow NS, Yokoyama S (1999) Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics 153:1839–1850

    PubMed  CAS  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    PubMed  CAS  Google Scholar 

  • Kodric-Brown A (1985) Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 17:199–205

    Article  Google Scholar 

  • 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 69:54–65

    Article  Google Scholar 

  • 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 305:567–580

    Article  PubMed  CAS  Google Scholar 

  • Lindholm AK, Brooks R, Breden F (2004) Extreme polymorphism in a Y-linked sexually selected trait. Heredity 92:156–162

    Article  PubMed  CAS  Google Scholar 

  • 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 28:1083–1093

    Article  PubMed  CAS  Google Scholar 

  • Loew ER (1994) A third, ultraviolet-sensitive, visual pigment in the Tokay Gecko (Gecko gekko). Vis Res 34:1427–1431

    Article  PubMed  CAS  Google Scholar 

  • MacNichol EF (1986) A unifying presentation of photopigment spectra. Vis Res 26:1543–1556

    Article  PubMed  CAS  Google Scholar 

  • Mansai SP, Innan H (2010) The power of the methods for detecting interlocus gene conversion. Genetics 184:517–527

    Article  PubMed  CAS  Google Scholar 

  • 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–D210

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto Y, Fukamach S, Mitam H, Kawamura S (2006) Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371:268–278

    Article  PubMed  CAS  Google Scholar 

  • 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 55:631–639

    Article  PubMed  Google Scholar 

  • Neafsey DE, Hartl DL (2005) Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon pufferfish lineages. Gene 350:161–171

    Article  PubMed  CAS  Google Scholar 

  • Ning ZM, Cox AJ, Mullikin JC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11:1725–1729

    Article  PubMed  CAS  Google Scholar 

  • Nylander JA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden

    Google Scholar 

  • 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 24:581–583

    Article  PubMed  CAS  Google Scholar 

  • 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:e5970

    Article  PubMed  Google Scholar 

  • Press W, Flannery B, Teukolsky S, Vetterling W (1987) Numerical recipes in Pascal. Cambridge University Press, Cambridge

    Google Scholar 

  • 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–D65

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A (1996) Se-Al: sequence alignment editor. http://evolve.zoo.ox.ac.uk

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer

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

    Article  PubMed  CAS  Google Scholar 

  • Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9

    Article  PubMed  CAS  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    CAS  Google Scholar 

  • 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 99:1008–1011

    Article  PubMed  CAS  Google Scholar 

  • 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 23:1538–1547

    Article  PubMed  CAS  Google Scholar 

  • Suzek BE, Huang HZ, McGarvey P, Mazumder R, Wu CH (2007) UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23:1282–1288

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic analysis using Parsimony (*and Other Methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244

    Article  CAS  Google Scholar 

  • 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 276:2195–2208

    Article  PubMed  CAS  Google Scholar 

  • 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 182:365–374

    Article  PubMed  CAS  Google Scholar 

  • 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 104:12813–12818

    Article  PubMed  CAS  Google Scholar 

  • 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 25:257–264

    Article  PubMed  Google Scholar 

  • 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 9:429–440

    Article  PubMed  CAS  Google Scholar 

  • 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 8:210

    Article  PubMed  Google Scholar 

  • 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 10:87

    Article  PubMed  Google Scholar 

  • 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):S11

    Article  PubMed  Google Scholar 

  • 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 19:968–984

    Article  PubMed  Google Scholar 

  • Windsor DJ, Owens GL (2009) The opsin repertoire of Jenynsia onca: a new perspective on gene duplication and divergence in livebearers. BMC Res Notes 2:159

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama S, Radlwimmer B (1998) The “five-sites” rule and the evolution of red and green color vision in mammals. Mol Biol Evol 15:560–567

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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 87:9315–9318

    Article  PubMed  CAS  Google Scholar 

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Watson, C.T., Gray, S.M., Hoffmann, M. et al. Gene Duplication and Divergence of Long Wavelength-Sensitive Opsin Genes in the Guppy, Poecilia reticulata . J Mol Evol 72, 240–252 (2011). https://doi.org/10.1007/s00239-010-9426-z

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