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 Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  Laver, Christopher Rj ^a   Taylor, John S ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE CLASS; COLOR MORPH; COURTSHIP; CYPRINID; DIVERGENCE; EYE; GENE EXPRESSION; JUVENILE; MATE CHOICE; PHOTORECEPTION; PIGMENT; POLYMERASE CHAIN REACTION; REAL TIME; SEXUAL SELECTION; SPERM COMPETITION; VISION;

CYPRINODONTIFORMES; POECILIA RETICULATA;

FISH PROTEIN; OPSIN;

ANIMAL; ARTICLE; CYPRINODONTIFORMES; EVALUATION; EYE; FEMALE; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MATE CHOICE; METABOLISM; METHODOLOGY; PHYSIOLOGY; PIGMENTATION; POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT; TIME; UPREGULATION; VISION;

ANIMALS; EYE; FEMALE; FISH PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MATING PREFERENCE, ANIMAL; OPSINS; PIGMENTATION; POECILIA; POLYMERASE CHAIN REACTION; SELECTION, GENETIC; SEX CHARACTERISTICS; TIME FACTORS; UP-REGULATION; VISION, OCULAR;

EID: 79953070182     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-81     Document Type: Article

References (95)

1. The location of eighteen genes in Lebistes reticulatus. O Winge, Journal of Genetics 1927 18 1 43 10.1007/BF03052599
2. Natural and sexual selection on color patterns in poeciliid fishes. JA Endler, Environmental Biology of Fishes 1983 9 173 190 10.1007/BF00690861 (Pubitemid 14275489)
3. Natural selection on color patterns in Poecilia reticulata. JA Endler, Evolution 1980 34 76 91 10.2307/2408316
4. Mate choice based upon naturally occurring color-pattern variation in a guppy population. AE Houde, Evolution 1987 41 1 10 10.2307/2408968
5. Directional postcopulatory sexual selection revealed by artificial insemination. JP Evans L Zane S Francescato A Pilastro, Nature 2003 421 360 363 10.1038/nature01367 12540898 (Pubitemid 36157931)
6. Opsin gene duplication and diversification in the guppy, a model for sexual selection. M Hoffmann N Tripathi SR Henz AK Lindholm D Weigel F Breden C Dreyer, Proc Biol Sci 2007 274 33 42 10.1098/rspb.2006.3707 17015333 (Pubitemid 47055493)
7. Long-wavelength sensitive visual pigments of the guppy (Poecilia reticulata): Six opsins expressed in a single individual. CJ Weadick BSW Chang, BMC Evolutionary Biology 2007 7 suppl 1 1 S11 10.1186/1471-2148-7-S1-S11 (Pubitemid 351814013)
8. 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. MN Ward AM Churcher KJ Dick CR Laver GL Owens MD Polack PR Ward F Breden JS Taylor, BMC Evol Biol 2008 8 210 10.1186/1471-2148-8-210 18638376
9. Role of predation in evolution of social-behavior of natural-populations of guppy, Poecilia-reticulata (pisces-poeciliidae). JA Farr, Evolution 1975 29 151 158 10.2307/2407148
10. Variation in the demography of guppy populations: The importance of predation and life histories. FH Rodd DN Reznick, Ecology 1997 78 405 418
11. Phenotypic plasticity in the life history traits of guppies: Responses to social environment. FH Rodd DN Reznick MB Sokolowski, Ecology 1997 78 419 433 10.1890/0012-9658(1997)078[0419:PPITLH]2.0.CO;2
12. Life-history evolution in guppies (Poecilia reticulata: Poeciliidae).5. Genetic basis of parallelism in life histories. DN Reznick HA Bryga, American Naturalist 1996 147 339 359 10.1086/285855 (Pubitemid 3042926)
13. Life-history evolution in guppies (Poecilia reticulata).6. Differential mortality as a mechanism for natural selection. DN Reznick MJ Butler FH Rodd P Ross, Evolution 1996 50 1651 1660 10.2307/2410901
14. Geographic-variation in the sexual-behavior of the guppy, Poecilia reticulata (peters). PH Luyten NR Liley, Behaviour 1985 95 164 179 10.1163/156853985X00109
15. A predator's view of animal color patterns. JA ENDLER, Evolutionary Biology 1978 11 319 364
16. Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. JA Endler, Vision Res 1991 31 587 608 10.1016/0042-6989(91)90109-I 1843763
17. Evolution of the vertebrate eye: Opsins, photoreceptors, retina and eye cup. TD Lamb SP Collin EN Pugh Jr, Nat Rev Neurosci 2007 8 960 976 10.1038/nrn2283 18026166 (Pubitemid 350147904)
18. Evolution of vertebrate retinal photoreception. TD Lamb, Philosophical Transactions of the Royal Society B-Biological Sciences 2009 364 2911 2924 10.1098/rstb.2009.0102
19. Molecular evolution of vertebrate visual pigments. S Yokoyama, Prog Retin Eye Res 2000 19 385 419 10.1016/S1350-9462(00)00002-1 10785616 (Pubitemid 30214233)
20. Ancient colour vision: Multiple opsin genes in the ancestral vertebrates. SP Collin MA Knight WL Davies IC Potter DM Hunt AE Trezise, Curr Biol 2003 13 864 865 10.1016/j.cub.2003.10.044 14614838 (Pubitemid 37425191)
21. Primary structures of chicken cone visual pigments: Vertebrate rhodopsins have evolved out of cone visual pigments. T Okano D Kojima Y Fukada Y Shichida T Yoshizawa, Proc Natl Acad Sci USA 1992 89 5932 5936 10.1073/pnas.89.13.5932 1385866
22. The evolution of early vertebrate photoreceptors. SP Collin WL Davies NS Hart DM Hunt, Philos Trans R Soc Lond B Biol Sci 2009 364 2925 2940 10.1098/rstb.2009.0099 19720654
23. Evolution and spectral tuning of visual pigments in birds and mammals. DM Hunt LS Carvalho JA Cowing WL Davies, Philos Trans R Soc Lond B Biol Sci 2009 364 2941 2955 10.1098/rstb.2009.0044 19720655
24. A fish eye out of water: Ten visual opsins in the four-eyed fish, anableps anableps. GL Owens DJ Windsor J Mui JS Taylor, PLoS One 2009 4 5970 10.1371/journal.pone.0005970 19551143
25. Visual pigment polymorphism in the guppy Poecilia reticulata. SN Archer JA Endler JN Lythgoe JC Partridge, Vision Res 1987 27 1243 1252 10.1016/0042-6989(87)90200-8 3424671
26. The visual pigment basis for cone polymorphism in the guppy, Poecilia reticulata. SN Archer JN Lythgoe, Vision Res 1990 30 225 233 10.1016/0042-6989(90)90038-M 2309457 (Pubitemid 20033253)
27. Variation in response to artificial selection for light sensitivity in guppies (Poecilia reticulata). JA Endler A Basolo S Glowacki J Zerr, Am Nat 2001 158 36 48 10.1086/320862 18707313 (Pubitemid 32550578)
28. Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish. CM Hofmann KL Carleton, Integrative and Comparative Biology 2009 49 630 643 10.1093/icb/icp079
29. Opsins: Evolution in waiting. AE Trezise SP Collin, Curr Biol 2005 15 794 796 10.1016/j.cub.2005.09.025 16213808 (Pubitemid 41415618)
30. Emergence of novel color vision in mice engineered to express a human cone photopigment. GH Jacobs GA Williams H Cahill J Nathans, Science 2007 315 1723 1725 10.1126/science.1138838 17379811 (Pubitemid 46515628)
31. Gene therapy for red-green colour blindness in adult primates. K Mancuso WW Hauswirth Q Li TB Connor JA Kuchenbecker MC Mauck J Neitz M Neitz, Nature 2009 461 784 787 10.1038/nature08401 19759534
32. Females prefer carotenoid colored males as mates in the pentamorphic livebearing fish, Poecilia parae. GR Bourne F Breden TC Allen, Naturwissenschaften 2003 90 402 405 10.1007/s00114-003-0444-1 14504782 (Pubitemid 37255542)
33. Consensus among females in their choice of males in the guppy Poecilia reticulata. A Kodric-Brown PF Nicoletto, Behavioral Ecology and Sociobiology 1996 39 395 400 10.1007/s002650050306 (Pubitemid 27047723)
34. Female choice in the guppy (Poecilia reticulata): The interaction between male color and display. A Kodric-Brown PF Nicoletto, Behavioral Ecology and Sociobiology 2001 50 346 351 10.1007/s002650100374 (Pubitemid 32895131)
35. Gene duplication and divergence of long wavelength-sensitive opsin genes in the guppy, Poecilia reticulata. CT Watson SM Gray M Hoffmann KP Lubieniecki JB Joy BA Sandkam D Weigel E Loew C Dreyer WS Davidson F Breden, Journal of Molecular Evolution 2010 21170644
36. Position of a 'green-red' hybrid gene in the visual pigment array determines colour-vision phenotype. T Hayashi AG Motulsky SS Deeb, Nature Genetics 1999 22 90 93 10.1038/8798 10319869 (Pubitemid 29214812)
37. Selective expression of human × chromosome-linked green opsin genes. J Winderickx L Battisti AG Motulsky SS Deeb, Proc Natl Acad Sci USA 1992 89 9710 9714 10.1073/pnas.89.20.9710 1409688
38. Identification of a locus control region for quadruplicated green-sensitive opsin genes in zebrafish. T Tsujimura A Chinen S Kawamura, Proc Natl Acad Sci USA 2007 104 12813 12818 10.1073/pnas.0704061104 17646658 (Pubitemid 47255237)
39. Diurnal rhythm of cone opsin expression in the teleost fish Haplochromis burtoni. S Halstenberg KM Lindgren SP Samagh M Nadal-Vicens S Balt RD Fernald, Vis Neurosci 2005 22 135 141 10.1017/S0952523805222022 15935106 (Pubitemid 40897398)
40. Circadian rhythms of behavioral cone sensitivity and long wavelength opsin mrna expression: A correlation study in zebrafish. P Li S Temple Y Gao TJ Haimberger CW Hawryshyn L Li, J Exp Biol 2005 208 497 504 10.1242/jeb.01424 15671338 (Pubitemid 40307432)
41. Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. CT Watson KP Lubieniecki E Loew WS Davidson F Breden, Bmc Evolutionary Biology 2010 10 10.1186/1471-2148-10-87 20353595
42. Evolution of vertebrate visual pigments. JK Bowmaker, Vision Research 2008 48 2022 2041 10.1016/j.visres.2008.03.025 18590925
43. JK Bowmaker ER Loew, The senses: A comprehensive reference Boston: Elsevier 2008
44. Intraretinal distribution of cone pigments in certain teleost fishes. JS Levine EF MacNichol Jr T Kraft BA Collins, Science 1979 204 523 526 10.1126/science.432658 432658 (Pubitemid 9186283)
45. Ellipsosomes: Organelles containing a cytochrome-like pigment in the retinal cones of certain fishes. EF MacNichol Jr YW Kunz JS Levine FI Harosi BA Collins, Science 1978 200 549 552 10.1126/science.644317 644317 (Pubitemid 8328389)
46. Structural differences of cone oil-droplets in light and dark adapted retina of Poecilia-reticulata-p. YW Kunz C Wise, Experientia 1978 34 246 249 10.1007/BF01944706 (Pubitemid 8273961)
47. Retinal ellipsosomes: Morphology, development, identification, and comparison with oil droplets. TC Nag J Bhattacharjee, Cell Tissue Res 1995 279 633 637 10.1007/BF00318176 7736559
48. The molecular genetics and evolution of red and green color vision in vertebrates. S Yokoyama FB Radlwimmer, Genetics 2001 158 1697 1710 11545071 (Pubitemid 32783150)
49. The "Five-sites" Rule and the evolution of red and green color vision in mammals. S Yokoyama B Radlwimmer, Molecular Biology and Evolution 1998 15 560 567 9580985 (Pubitemid 28194620)
50. Visual pigments in teleost fishes: Effects of habitat, microhabitat, and behavior on visual system evolution. J Levine EJ MacNichol, Sensory Processes 1979 3 95 131 545702 (Pubitemid 10047463)
51. Visual communication in fishes. JS Levine PS Lobel EF MacNichol, Environmental physiology of fishes New York: Plenum Press, Ali MA, 1979 447 475
52. Functional characterization of visual opsin repertoire in medaka (Oryzias latipes). Y Matsumoto S Fukamach H Mitam S Kawamura, Gene 2006 371 268 278 10.1016/j.gene.2005.12.005 16460888
53. Genetic and environmental variation in the visual properties of bluefin killifish, Lucania goodei. RC Fuller KL Carleton JM Fadool TC Spady J Travis, J Evol Biol 2005 18 516 523 10.1111/j.1420-9101.2005.00886.x 15842481 (Pubitemid 40654074)
54. Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. WL Davies SP Collin DM Hunt, Molecular Biology and Evolution 2009 26 1803 1809 10.1093/molbev/msp089 19398493
55. The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, acanthopagrus butcheri. J Shand WL Davies N Thomas L Balmer JA Cowing M Pointer LS Carvalho AE Trezise SP Collin LD Beazley DM Hunt, J Exp Biol 2008 211 1495 1503 10.1242/jeb.012047 18424684 (Pubitemid 351954833)
56. Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. TC Spady JWL Parry PR Robinson DM Hunt JK Bowmaker KL Carleton, Molecular Biology and Evolution 2006 23 1538 1547 10.1093/molbev/msl014 16720697 (Pubitemid 44297412)
57. Cone mosaics in a teleost retina: Changes during light and dark adaptation. YW Kunz, Experientia 1980 36 1371 1374 10.1007/BF01960104 7202641 (Pubitemid 11185249)
58. Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). WT Allison SG Dann JV Helvik C Bradley HD Moyer CW Hawryshyn, Journal of Comparative Neurology 2003 461 294 306 10.1002/cne.10682 12746869 (Pubitemid 36648069)
59. Gene duplication and spectral diversification of cone visual pigments of zebrafish. A Chinen T Hamaoka Y Yamada S Kawamura, Genetics 2003 163 663 675 12618404 (Pubitemid 36314548)
60. Spatio-temporal characterization of retinal opsin gene expression during thyroid hormone-induced and natural development of rainbow trout. K Veldhoen WT Allison N Veldhoen BR Anholt CC Helbing CW Hawryshyn, Visual Neuroscience 2006 23 169 179 10.1017/S0952523806232139 16638170
61. A difference between rods and cones in renewal of outer segment protein. RW Young, Investigative Ophthalmology 1969 8 222-&
62. Circadian rhythm and light regulate opsin mrna in rod photoreceptors. JI Korenbrot RD Fernald, Nature 1989 337 454 457 10.1038/337454a0 2521689 (Pubitemid 19047461)
63. Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. M Takechi S Kawamura, J Exp Biol 2005 208 1337 1345 10.1242/jeb.01532 15781894 (Pubitemid 40564568)
64. Geographic-variation in female preferences for male traits in Poecilia reticulata. JA Endler AE Houde, Evolution 1995 49 456 468 10.2307/2410270 (Pubitemid 26448901)
65. Signals, signal conditions, and the direction of evolution. JA Endler, American Naturalist 1992 139 125 S153 10.1086/285308
66. Color vision in fishes. JS Levine EF MacNichol Jr, Scientific American 1982 246 108 117
67. Ethological studies on Lebistes reticulatus (peters) 1. An analysis of the male courtship pattern. GP Baerends R Brouwer HT Waterbolk, Behaviour 1955 8 249 334 10.1163/156853955X00238
68. Ethological isolating mechanisms in four sympatric species of poeciliid fishes. NR Liley, Behaviour Supplement 1965 1 197
69. Visual pigment coexpression in all cones of two rodents, the siberian hamster, and the pouched mouse. A Lukats O Dkhissi-Benyahya Z Szepessy P Rohlich B Vigh NC Bennett HM Cooper A Szel, Invest Ophthalmol Vis Sci 2002 43 2468 2473 12091452 (Pubitemid 34700683)
70. Spectral sensitivity of single cones in rainbow trout (Oncorhynchus mykiss): A whole-cell voltage clamp study. L Anderson S Sabbah C Hawryshyn, Vision Research 2010 50 2055 2061 10.1016/j.visres.2010.07.013 20655939
71. Human photoreceptor topography. CA Curcio KR Sloan RE Kalina AE Hendrickson, Journal of Comparative Neurology 1990 292 497 523 10.1002/cne.902920402 2324310 (Pubitemid 20076633)
72. Seeing with s cones. DJ Calkins, Progress in Retinal and Eye Research 2001 20 255 287 10.1016/S1350-9462(00)00026-4 11286894 (Pubitemid 32245683)
73. Visual pigments and molecular genetics of color blindness. JK Bowmaker, News Physiol Sci 1998 13 63 69 11390764
74. Evolution of vertebrate visual pigments. JK Bowmaker, Vision Res 2008 48 2022 2041 10.1016/j.visres.2008.03.025 18590925
75. Dietary carotenoids and male mating success in the guppy: An environmental component to female choice. A Kodric-Brown, Behavioral Ecology and Sociobiology 1989 25 393 401 10.1007/BF00300185
76. Carotenoid limitation and mate preference evolution: A test of the indicator hypothesis in guppies (Poecilia reticulata). GF Grether, Evolution 2000 54 1712 1724 11108598
77. A possible non-sexual origin of mate preference: Are male guppies mimicking fruit? FH Rodd KA Hughes GF Grether CT Baril, Proc Biol Sci 2002 269 475 481 10.1098/rspb.2001.1891 11886639 (Pubitemid 34264045)
78. Maternal effects of carotenoid consumption in guppies (Poecilia reticulata). GF Grether GR Kolluru K Lin MA Quiroz G Robertson AJ Snyder, Functional Ecology 2008 22 294 302 10.1111/j.1365-2435.2007.01365.x (Pubitemid 351416628)
79. Algal-searching ability in laboratory experiments reflects orange spot coloration of the male guppy in the wild. K Karino S Shinjo A Sato, Behaviour 2007 144 101 113 10.1163/156853907779947427 (Pubitemid 47190459)
80. Sex-specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata). GF Grether S Kasahara GR Kolluru EL Cooper, Proceedings of the Royal Society of London Series B-Biological Sciences 2004 271 45 49 10.1098/rspb.2003.2526 (Pubitemid 38100506)
81. Effect of parasitic infection on male color pattern and female choice in guppies. AE Houde AJ Torio, Behavioral Ecology 1992 3 346 351 10.1093/beheco/3.4.346
82. Beauty in the eye of the beholder: The two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes. MP Sison-Mangus GD Bernard J Lampel AD Briscoe, Journal of Experimental Biology 2006 209 3079 3090 10.1242/jeb.02360 16888057 (Pubitemid 44476233)
83. Spectral irradiance and foraging efficiency in the guppy, Poecilia reticulata. EM White SC Church LJ Willoughby SJ Hudson JC Partridge, Animal Behaviour 2005 69 519 527 10.1016/j.anbehav.2004.05.011 (Pubitemid 40253016)
84. Cone visual pigments of monotremes: Filling the phylogenetic gap. MJ Wakefield M Anderson E Chang KJ Wei R Kaul JAM Graves F Grutzner SS Deeb, Visual Neuroscience 2008 25 257 264 10.1017/S0952523808080255 18598396 (Pubitemid 351948106)
85. Rna-based gene duplication: Mechanistic and evolutionary insights. H Kaessmann N Vinckenbosch MY Long, Nature Reviews Genetics 2009 10 19 31 10.1038/nrg2487 19030023
86. The opsin repertoire of jenynsia onca: A new perspective on gene duplication and divergence in livebearers. DJ Windsor GL Owens, BMC Res Notes 2009 2 159 10.1186/1756-0500-2-159 19656397
87. Gephyrin, a major postsynaptic protein of gabaergic synapses. M Sassoe-Pognetto JM Fritschy, European Journal of Neuroscience 2000 12 2205 2210 10.1046/j.1460-9568.2000.00106.x 10947798 (Pubitemid 30497017)
88. Mechanisms underlying lateral gabaergic feedback onto rod bipolar cells in rat retina. AE Chavez WN Grimes JS Diamond, Journal of Neuroscience 2010 30 2330 2339 10.1523/JNEUROSCI.5574-09.2010 20147559
89. Cone droplets of mitochondrial origin in retina of Fundulus-heteroclitus (pisces-cyprinodontidae). M Anctil MA Ali, Zoomorphologie 1976 84 103 111 10.1007/BF02568559
90. Ultrastructural diurnal changes of the retinal photoreceptors in the embryo of a viviparous teleost (Poecilia reticulata p.). YW Kunz S Ennis, Cell Differ 1983 13 115 123 10.1016/0045-6039(83)90103-3 6686498 (Pubitemid 14201667)
91. Ontogeny of the photoreceptors in the embryonic retina of the viviparous guppy, Poecilia reticulata p. (teleostei). An electron-microscopical study. YW Kunz S Ennis C Wise, Cell Tissue Res 1983 230 469 486 10.1007/BF00216193 6850777 (Pubitemid 13136255)
92. Development of the photoreceptors in the embryonic retina of Lebistes reticulatus (peters). Electron microscopical investigations. (with 7 figures). YW Kunz C Wise, Rev Suisse Zool 1974 81 697 701 4445817
93. Regional differences of argentea and sclera in eye of Poecilia-reticulata-p (teleostei-cyprinodontidae) - light-microscopic and electron-microscopic study. YW Kunz C Wise, Zoomorphologie 1977 87 203 215 10.1007/BF00995820
94. 'disk shedding' in the cone outer segments of the teleost, Poecilia reticulata p. A Yacob YW Kunz, Cell Tissue Res 1977 181 487 492 10.1007/BF00221770 884718 (Pubitemid 8143478)
95. The accessory outer segment of rods and cones in the retina of the guppy, Poecilia reticulata p. (teleostei). An electron microscopical study. A Yacob C Wise YW Kunz, Cell Tissue Res 1977 177 181 193 10.1007/BF00221080 837406 (Pubitemid 8062508)