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Annual Review of Cell and Developmental Biology

Volume 37, 2021

The Visual Opsin Gene Repertoires of Teleost Fishes: Evolution, Ecology, and Function

Abstract

Visual opsin genes expressed in the rod and cone photoreceptor cells of the retina are core components of the visual sensory system of vertebrates. Here, we provide an overview of the dynamic evolution of visual opsin genes in the most species-rich group of vertebrates, teleost fishes. The examination of the rich genomic resources now available for this group reveals that fish genomes contain more copies of visual opsin genes than are present in the genomes of amphibians, reptiles, birds, and mammals. The expansion of opsin genes in fishes is due primarily to a combination of ancestral and lineage-specific gene duplications. Following their duplication, the visual opsin genes of fishes repeatedly diversified at the same key spectral-tuning sites, generating arrays of visual pigments sensitive to the ultraviolet to red spectrum of light. Species-specific opsin gene repertoires correlate strongly with underwater light habitats, ecology, and color-based sexual selection.

Keyword(s): eye, fish vision, gene duplication, key spectral-tuning sites, photoreceptor cell, retina
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/content/journals/10.1146/annurev-cellbio-120219-024915
2021-10-06
2024-04-19
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Literature Cited

  1. Aardema ML, Stiassny MLJ, Alter SE. 2020. Genomic analysis of the only blind cichlid reveals extensive inactivation in eye and pigment formation genes. Genome Biol. Evol. 12:81392–406
     [Google Scholar]
  2. Adrian-Kalchhauser I, Blomberg A, Larsson T, Musilova Z, Peart CR et al. 2020. The round goby genome provides insights into mechanisms that may facilitate biological invasions. BMC Biol 18:11
     [Google Scholar]
  3. Ali M-A, Anctil M. 1976. Retinas of Fishes: An Atlas Berlin/Heidelberg: Springer
  4. Alvarez-Delfin K, Morris AC, Snelson CD, Gamse JT, Gupta T et al. 2009. Tbx2b is required for ultraviolet photoreceptor cell specification during zebrafish retinal development. PNAS 106:62023–28
     [Google Scholar]
  5. Archer S, Hope A, Partridge JC. 1995. The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proc. R. Soc. B 262: 1365.289–95
     [Google Scholar]
  6. Arshavsky VY, Lamb TD, Pugh EN. 2002. G proteins and phototransduction. Annu. Rev. Physiol. 64:153–87
     [Google Scholar]
  7. Baden T, Euler T, Berens P. 2020. Understanding the retinal basis of vision across species. Nat. Rev. Neurosci. 21:5–20
     [Google Scholar]
  8. Bellingham J, Tarttelin EE, Foster RG, Wells DJ. 2003. Structure and evolution of the teleost extraretinal rod-like opsin (errlo) and ocular rod opsin (rho) genes: Is teleost rho a retrogene?. J. Exp. Zool. B Mol. Dev. Evol. 297B:11–10
     [Google Scholar]
  9. Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N et al. 2017. Phylogenetic classification of bony fishes. BMC Evol. Biol. 17:162
     [Google Scholar]
  10. Boughman JW. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:6840944–48
     [Google Scholar]
  11. Bowmaker JK. 1995. The visual pigments of fish. Prog. Retin. Eye Res. 15:11–31
     [Google Scholar]
  12. Bowmaker JK. 2008. Evolution of vertebrate visual pigments. Vis. Res. 48:202022–41
     [Google Scholar]
  13. Browman HI, Novales Flamarique H, Hawryshyn C 1994. Ultraviolet photoreception contributes to prey search behaviour in two species of zooplanktivorous fishes. J. Exp. Biol. 186:187–98
     [Google Scholar]
  14. Carleton KL, Escobar-Camacho D, Stieb SM, Cortesi F, Marshall NJ. 2020. Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes. J. Exp. Biol. 223:8jeb193334
     [Google Scholar]
  15. Carleton KL, Spady TC, Streelman JT, Kidd MR, McFarland WN, Loew ER. 2008. Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol 6:22
     [Google Scholar]
  16. Carleton KL, Yourick MR. 2020. Axes of visual adaptation in the ecologically diverse family Cichlidae. Semin. Cell Dev. Biol 106:43–52
     [Google Scholar]
  17. Castiglione GM, Hauser FE, Liao BS, Lujan NK, Van Nynatten A et al. 2017. Evolution of nonspectral rhodopsin function at high altitudes. PNAS 114:287385–90
     [Google Scholar]
  18. Chang BS, Donoghue MJ. 2000. Recreating ancestral proteins. Trends Ecol. Evol. 15:3109–114
     [Google Scholar]
  19. Chen J-N, Samadi S, Chen W-J. 2018. Rhodopsin gene evolution in early teleost fishes. PLOS ONE 13:11e0206918
     [Google Scholar]
  20. Cheng CL, Gan KJ, Novales Flamarique I 2007. The ultraviolet opsin is the first opsin expressed during retinal development of salmonid fishes. Investig. Opthalmol. Vis. Sci. 48:2866
     [Google Scholar]
  21. Cheng CL, Novales Flamarique I 2004. New mechanism for modulating colour vision. Nature 428:6980279–79
     [Google Scholar]
  22. Clark CW, Levy DA. 1988. Diel vertical migrations by juvenile sockeye salmon and the antipredation window. Am. Nat. 131:2271–90
     [Google Scholar]
  23. Collin SP 2009. Evolution of the visual system in fishes. Encyclopedia of Neuroscience MD Binder, N Hirokawa, U Windhorst 1459–66 Berlin/Heidelberg: Springer
     [Google Scholar]
  24. Cortesi F, Cheney KM, Cooke GM, Ord T. 2018. Opsin gene evolution in amphibious and terrestrial combtooth blennies (Blenniidae). bioRxiv 503516. https://doi.org/10.1101/503516
    [Crossref]
  25. Cortesi F, Escobar Camacho D, Luehrmann M, Sommer GM, Musilova Z 2021. Multiple ancestral duplications of the red-sensitive opsin gene (LWS) in teleost fishes and convergent spectral shifts to green vision in gobies. bioRxiv 443214. https://doi.org/10.1101/2021.05.08.443214
    [Crossref]
  26. Cortesi F, Mitchell LJ, Tettamanti V, Fogg LG, de Busserolles F et al. 2020. Visual system diversity in coral reef fishes. Semin. Cell Dev. Biol 106:31–42
     [Google Scholar]
  27. Cortesi F, Musilová Z, Stieb SM, Hart NS, Siebeck UE et al. 2015. Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes. PNAS 112:51493–98
     [Google Scholar]
  28. Cortesi F, Musilová Z, Stieb SM, Hart NS, Siebeck UE et al. 2016. From crypsis to mimicry: changes in colour and the configuration of the visual system during ontogenetic habitat transitions in a coral reef fish. J. Exp. Biol. 219:162545–58
     [Google Scholar]
  29. Cronin TW, Caldwell RL, Marshall J. 2001. Tunable colour vision in a mantis shrimp. Nature 411:6837547–48
     [Google Scholar]
  30. Cronin TW, Johnsen S, Marshall J, Warrant EJ 2014. Visual Ecology Princeton, NJ: Princeton Univ. Press
  31. Cummings ME, Endler JA. 2018. 25 years of sensory drive: the evidence and its watery bias. Curr. Zool. 64:4471–84
     [Google Scholar]
  32. Cummings ME, Rosenthal GG, Ryan MJ. 2003. A private ultraviolet channel in visual communication. Proc. R. Soc. B 270: 1518.897–904
     [Google Scholar]
  33. Dalton BE, Loew ER, Cronin TW, Carleton KL. 2014. Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field. Proc. R. Soc. B 281: 1797.20141980
     [Google Scholar]
  34. Dalton BE, Lu J, Leips J, Cronin TW, Carleton KL. 2015. Variable light environments induce plastic spectral tuning by regional opsin coexpression in the African cichlid fish, Metriaclima zebra. Mol. Ecol. 24:164193–204
     [Google Scholar]
  35. de Busserolles F, Cortesi F, Fogg L, Stieb SM, Luehrmann M, Marshall NJ. 2021. The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina. J. Exp. Biol. 224:1jeb233098
     [Google Scholar]
  36. de Busserolles F, Cortesi F, Helvik JV, Davies WIL, Templin RM et al. 2017. Pushing the limits of photoreception in twilight conditions: the rod-like cone retina of the deep-sea pearlsides. Sci. Adv. 3:11eaao4709
     [Google Scholar]
  37. de Busserolles F, Fogg L, Cortesi F, Marshall J. 2020. The exceptional diversity of visual adaptations in deep-sea teleost fishes. Semin. Cell Dev. Biol. 106:20–30
     [Google Scholar]
  38. Dong L, Wang X, Guo H, Zhang X, Zhang M, Tang W. 2020. Chromosome-level genome assembly of the endangered humphead wrasse Cheilinus undulates insight into unexpected expansion of opsin genes in fishes. Authorea Preprints. https://www.authorea.com/doi/full/10.22541/au.159986378.81705478
  39. Douglas RH, Partridge JC, Marshall NJ. 1998. The eyes of deep-sea fish I: lens pigmentation, tapeta and visual pigments. Prog. Retin. Eye Res. 17:4597–636
     [Google Scholar]
  40. Dungan SZ, Kosyakov A, Chang BSW. 2016. Spectral tuning of killer whale (Orcinus orca) rhodopsin: evidence for positive selection and functional adaptation in a cetacean visual pigment. Mol. Biol. Evol. 33:2323–36
     [Google Scholar]
  41. Eaton KM, Bernal MA, Backenstose NJC, Yule DL, Krabbenhoft TJ. 2020. Nanopore amplicon sequencing reveals molecular convergence and local adaptation of rhodopsin in Great Lakes salmonids. Genome Biol. Evol. 13:2evaa237
     [Google Scholar]
  42. Endler JA. 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139:S125–53
     [Google Scholar]
  43. Enright JM, Toomey MB, Sato S, Temple SE, Allen JR et al. 2015. Cyp27c1 red-shifts the spectral sensitivity of photoreceptors by converting vitamin A1 into A2. Curr. Biol. 25:233048–57
     [Google Scholar]
  44. Escobar-Camacho D, Carleton KL, Narain DW, Pierotti MER. 2020. Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning. Mol. Ecol. 29:122234–53
     [Google Scholar]
  45. Escobar-Camacho D, Pierotti MER, Ferenc V, Sharpe DMT, Ramos E et al. 2019. Variable vision in variable environments: the visual system of an invasive cichlid (Cichla monoculus) in Lake Gatun, Panama. J. Exp. Biol. 222:6jeb188300
     [Google Scholar]
  46. Escobar-Camacho D, Ramos E, Martins C, Carleton KL. 2017. The opsin genes of amazonian cichlids. Mol. Ecol. 26:51343–56
     [Google Scholar]
  47. Fain GL. 2020. Lamprey vision: photoreceptors and organization of the retina. Semin. Cell Dev. Biol. 106:5–11
     [Google Scholar]
  48. Fasick JI, Robinson PR. 2000. Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth. Vis. Neurosci. 17:5781–88
     [Google Scholar]
  49. Fujiyabu C, Sato K, Utari NML, Ohuchi H, Shichida Y, Yamashita T. 2019. Evolutionary history of teleost intron-containing and intron-less rhodopsin genes. Sci. Rep. 9:10653
     [Google Scholar]
  50. Fuller RC, Carleton KL, Fadool JM, Spady TC, Travis J. 2005. Genetic and environmental variation in the visual properties of bluefin killifish, Lucania goodei: evolvable sensory systems. J. Evol. Biol. 18:3516–23
     [Google Scholar]
  51. Fuller RC, Claricoates KM. 2011. Rapid light-induced shifts in opsin expression: finding new opsins, discerning mechanisms of change, and implications for visual sensitivity. Mol. Ecol. 20:163321–35
     [Google Scholar]
  52. Fuller RC, Fleishman LJ, Leal M, Travis J, Loew E 2003. Intraspecific variation in retinal cone distribution in the bluefin killifish, Lucania goodei. J. Comp. Physiol. A 189:8609–16
     [Google Scholar]
  53. Fuller RC, Noa LA, Strellner RS. 2010. Teasing apart the many effects of lighting environment on opsin expression and foraging preference in bluefin killifish. Am. Nat. 176:11–13
     [Google Scholar]
  54. Giske J, Aksnes DL, Baliño BM, Kaartvedt S, Lie U et al. 1990. Vertical distribution and trophic interactions of zooplankton and fish in Masfjorden, Norway. Sarsia 75:165–81
     [Google Scholar]
  55. Gore AV, Tomins KA, Iben J, Ma L, Castranova D et al. 2018. An epigenetic mechanism for cavefish eye degeneration. Nat. Ecol. Evol. 2:71155–60
     [Google Scholar]
  56. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K 2000. In search of the visual pigment template. Vis. Neurosci 17:509–28
     [Google Scholar]
  57. Härer A, Meyer A, Torres-Dowdall J. 2018. Convergent phenotypic evolution of the visual system via different molecular routes: how neotropical cichlid fishes adapt to novel light environments. Evol. Lett. 2:4341–54
     [Google Scholar]
  58. Härer A, Torres-Dowdall J, Meyer A. 2017. Rapid adaptation to a novel light environment: the importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.). Mol. Ecol. 26:205582–93
     [Google Scholar]
  59. Hawryshyn CW, Arnold MG, Chaisson DJ, Martin PC. 1989. The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Vis. Neurosci. 2:3247–54
     [Google Scholar]
  60. Helfman GS. 1986. Fish behaviour by day, night and twilight. The Behaviour of Teleost Fishes TJ Pitcher 366–87 Boston: Springer
     [Google Scholar]
  61. Helfman GS, Collette BB, Facey DE, Bowen BW 2009. The Diversity of Fishes: Biology, Evolution, and Ecology Chichester, UK: Blackwell, 2nd ed..
  62. Hill J, Enbody ED, Pettersson ME, Sprehn CG, Bekkevold D et al. 2019. Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin. PNAS 116:3718473–78
     [Google Scholar]
  63. Hofmann CM, O'Quin KE, Marshall NJ, Cronin TW, Seehausen O, Carleton KL. 2009. The eyes have it: regulatory and structural changes both underlie cichlid visual pigment diversity. PLOS Biol 7:12e1000266
     [Google Scholar]
  64. Hunt DM, Fitzgibbon J, Slobodyanyuk SJ, Bowmakers JK. 1996. Spectral tuning and molecular evolution of rod visual pigments in the species flock of cottoid fish in Lake Baikal. Vis. Res. 36:91217–24
     [Google Scholar]
  65. Hunt DM, Hankins MW, Collin SP, Marshall NJ. 2014. Evolution of Visual and Non-Visual Pigments Boston: Springer
  66. Ivanov IV, Mappes T, Schaupp P, Lappe C, Wahl S. 2018. Ultraviolet radiation oxidative stress affects eye health. J. Biophoton. 11:7e201700377
     [Google Scholar]
  67. Iwanicki TW, Novales Flamarique I, Ausiό J, Morris E, Taylor JS 2017. Fine-tuning light sensitivity in the starry flounder (Platichthys stellatus) retina: regional variation in photoreceptor cell morphology and opsin gene expression. J. Comp. Neurol. 525:102328–42
     [Google Scholar]
  68. Jeffery WR. 2009. Regressive evolution in Astyanax cavefish. Annu. Rev. Genet. 43:25–47
     [Google Scholar]
  69. Jerlov NG. 1976. Marine Optics Amsterdam: Elsevier, 2nd ed..
  70. Job S, Bellwood DR 2007. Ultraviolet photosensitivity and feeding in larval and juvenile coral reef fishes. Mar. Biol. 151:2495–503
     [Google Scholar]
  71. Jordan R, Howe D, Juanes F, Stauffer J, Loew E. 2004. Ultraviolet radiation enhances zooplanktivory rate in ultraviolet sensitive cichlids. Afr. J. Ecol. 42:3228–31
     [Google Scholar]
  72. Kim E-S, Lee C-H, Lee Y-D. 2019. Retinal development and opsin gene expression during the juvenile development in red spotted grouper (Epinephelus akaara). Dev. Reprod. 23:2171–81
     [Google Scholar]
  73. Krauskopf J, Williams DR, Heeley DW. 1982. Cardinal directions of color space. Vis. Res 22:91123–31
     [Google Scholar]
  74. Kröger RHH, Campbell MCW, Fernald RD, Wagner H-J. 1999. Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J. Comp. Physiol. A 184:4361–69
     [Google Scholar]
  75. Lamb TD. 2020. Evolution of the genes mediating phototransduction in rod and cone photoreceptors. Prog. Retin. Eye Res. 76:100823
     [Google Scholar]
  76. Lamb TD, Collin SP, Pugh EN. 2007. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat. Rev. Neurosci. 8:12960–76
     [Google Scholar]
  77. Land MF, Nilsson D-E. 2012. Animal Eyes Oxford, UK/New York: Oxford Univ. Press, 2nd ed..
  78. Larhammar D, Nordström K, Larsson TA. 2009. Evolution of vertebrate rod and cone phototransduction genes. Philos. Trans. R. Soc. B 364: 1531.2867–80
     [Google Scholar]
  79. Lin J-J, Wang F-Y, Li W-H, Wang T-Y. 2017. The rises and falls of opsin genes in 59 ray-finned fish genomes and their implications for environmental adaptation. Sci. Rep. 7:15568
     [Google Scholar]
  80. Liu D-W, Lu Y, Yan HY, Zakon HH. 2016. South American weakly electric fish (Gymnotiformes) are long-wavelength-sensitive cone monochromats. Brain Behav. Evol. 88:3–4204–12
     [Google Scholar]
  81. Liu D-W, Wang F-Y, Lin J-J, Thompson A, Lu Y et al. 2019. The cone opsin repertoire of osteoglossomorph fishes: gene loss in mormyrid electric fish and a long wavelength-sensitive cone opsin that survived 3R. Mol. Biol. Evol. 36:3447–57
     [Google Scholar]
  82. Loew ER, McFarland WN, Margulies D. 2002. Developmental changes in the visual pigments of the yellowfin tuna, Thunnus albacares. Mar. Freshw. Behav. Physiol. 35:4235–46
     [Google Scholar]
  83. Loew ER, McFarland WN, Mills EL, Hunter D. 1993. A chromatic action spectrum for planktonic predation by juvenile yellow perch, Perca flavescens. Can. J. Zool. 71:2384–86
     [Google Scholar]
  84. Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA, Marshall NJ. 2003. Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003:3433–54
     [Google Scholar]
  85. Luehrmann M, Carleton KL, Cortesi F, Cheney KL, Marshall NJ. 2019. Cardinalfishes (Apogonidae) show visual system adaptations typical of nocturnally and diurnally active fish. Mol. Ecol. 28:123025–41
     [Google Scholar]
  86. Luehrmann M, Cortesi F, Cheney KL, de Busserolles F, Marshall NJ. 2020. Microhabitat partitioning correlates with opsin gene expression in coral reef cardinalfishes (Apogonidae). Funct. Ecol. 34:51041–52
     [Google Scholar]
  87. Luehrmann M, Stieb SM, Carleton KL, Pietzker A, Cheney KL, Marshall NJ. 2018. Short-term colour vision plasticity on the reef: changes in opsin expression under varying light conditions differ between ecologically distinct fish species. J. Exp. Biol. 221:22jeb175281
     [Google Scholar]
  88. Luk HL, Bhattacharyya N, Montisci F, Morrow JM, Melaccio F et al. 2016. Modulation of thermal noise and spectral sensitivity in Lake Baikal cottoid fish rhodopsins. Sci. Rep. 6:38425
     [Google Scholar]
  89. Lupše N, Cortesi F, Freese M, Marohn L, Pohlman J-D et al. 2021. Visual gene expression reveals a cone to rod developmental progression in deep-sea fishes. bioRxiv 2020.05.25.114991 https://doi.org/10.1101/2020.05.25.114991
    [Crossref]
  90. Lythgoe JN. 1979. The Ecology of Vision Oxford, UK: Oxford Univ. Press
  91. Lythgoe JN, Muntz WRA, Partridge JC, Shand J, Williams DM. 1994. The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. J. Comp. Physiol. A 174:4461–67
     [Google Scholar]
  92. Mano H, Kojima D, Fukada Y. 1999. Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Mol. Brain Res. 73:1–2110–18
     [Google Scholar]
  93. Marques DA, Taylor JS, Jones FC, Di Palma F, Kingsley DM, Reimchen TE. 2017. Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments. PLOS Biol 15:4e2001627
     [Google Scholar]
  94. Marshall J, Carleton KL, Cronin T. 2015. Colour vision in marine organisms. Curr. Opin. Neurobiol. 34:86–94
     [Google Scholar]
  95. Marshall J, Kent J, Cronin T 1999. Visual adaptations in crustaceans: spectral sensitivity in diverse habitats. Adaptive Mechanisms in the Ecology of Vision SN Archer, MBA Djamgoz, ER Loew, JC Partridge, S Vallerga 285–327 Dordrecht, Neth: Springer
     [Google Scholar]
  96. Marshall J, Vorobiev M, Siebeck UE 2006. What does a reef fish see when it sees a reef fish?. Communication in Fishes, Vol. 1 F Ladich, SP Collin, P Moller, BG Kapoor 423–56 Enfield, NH: Sci. Publ.
     [Google Scholar]
  97. Marshall NJ, Cortesi F, de Busserolles F, Siebeck UE, Cheney KL. 2018. Colours and colour vision in reef fishes: past, present and future research directions. J. Fish Biol 95:15–38
     [Google Scholar]
  98. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS. 2003. Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003:3467–80
     [Google Scholar]
  99. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:2266–80
     [Google Scholar]
  100. McFarland WN. 1986. Light in the sea—correlations with behaviors of fishes and invertebrates. Am. Zool. 26:2389–401
     [Google Scholar]
  101. McGaugh SE, Gross JB, Aken B, Blin M, Borowsky R et al. 2014. The cavefish genome reveals candidate genes for eye loss. Nat. Commun. 5:5307
     [Google Scholar]
  102. Mehta TK, Koch C, Nash W, Knaack SA, Sudhakar P et al. 2021. Evolution of regulatory networks associated with traits under selection in cichlids. Genome Biol 22:25
     [Google Scholar]
  103. Meredith RW, Gatesy J, Emerling CA, York VM, Springer MS. 2013. Rod monochromacy and the coevolution of cetacean retinal opsins. PLOS Genet 9:4e1003432
     [Google Scholar]
  104. Meyer A, Van de Peer Y. 2005. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–45
     [Google Scholar]
  105. Michiels NK, Anthes N, Hart NS, Herler J, Meixner AJ et al. 2008. Red fluorescence in reef fish: a novel signalling mechanism?. BMC Ecol 8:16
     [Google Scholar]
  106. Mitchell LJ, Cheney KL, Chung W-S, Marshall NJ, Michie K, Cortesi F. 2020. Seeing Nemo: molecular evolution of ultraviolet visual opsins and spectral tuning of photoreceptors in anemonefishes (Amphiprioninae). bioRxiv 139766. https://doi.org/10.1101/2020.06.09.139766
    [Crossref]
  107. Miyagi R, Terai Y, Aibara M, Sugawara T, Imai H et al. 2012. Correlation between nuptial colors and visual sensitivities tuned by opsins leads to species richness in sympatric Lake Victoria cichlid fishes. Mol. Biol. Evol. 29:113281–96
     [Google Scholar]
  108. Morrow JM, Lazic S, Dixon Fox M, Kuo C, Schott RK et al. 2017. A second visual rhodopsin gene, rh1–2, is expressed in zebrafish photoreceptors and found in other ray-finned fishes. J. Exp. Biol. 220:2294–303
     [Google Scholar]
  109. Muntz WRA. 1973. Yellow filters and the absorption of light by the visual pigments of some amazonian fishes. Vis. Res. 13:122235–54
     [Google Scholar]
  110. Muntz WRA. 1976. Visual pigments of cichlid fishes from Malawi. Vis. Res. 16:9897–903
     [Google Scholar]
  111. Munz FW, McFarland WN. 1973. The significance of spectral position in the rhodopsins of tropical marine fishes. Vis. Res. 13:101829-IN1
     [Google Scholar]
  112. Munz FW, McFarland WN 1977. Evolutionary adaptations of fishes to the photic environment. The Visual System in Vertebrates F Crescitelli, CA Dvorak, DJ Eder, AM Granda, D Hamasaki et al.193–274 Berlin/Heidelberg: Springer
     [Google Scholar]
  113. Musilova Z, Cortesi F. 2021. Multiple ancestral and a plethora of recent gene duplications during the evolution of the green sensitive opsin genes (RH2) in teleost fishes.. bioRxiv 443711. https://doi.org/10.1101/2021.05.11.443711
    [Crossref] [Google Scholar]
  114. Musilova Z, Cortesi F, Matschiner M, Davies WIL, Patel JS et al. 2019a. Vision using multiple distinct rod opsins in deep-sea fishes. Science 364:6440588–92
     [Google Scholar]
  115. Musilova Z, Indermaur A, Bitja-Nyom AR, Omelchenko D, Kłodawska M et al. 2019b. Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon. Mol. Ecol. 28:235010–31
     [Google Scholar]
  116. Nandamuri SP, Yourick MR, Carleton KL. 2017. Adult plasticity in African cichlids: rapid changes in opsin expression in response to environmental light differences. Mol. Ecol. 26:216036–52
     [Google Scholar]
  117. Nilsson D-E. 2013. Eye evolution and its functional basis. Vis. Neurosci. 30:1–25–20
     [Google Scholar]
  118. Novales Flamarique I 2013. Opsin switch reveals function of the ultraviolet cone in fish foraging. Proc. R. Soc. B 280: 1752.20122490
     [Google Scholar]
  119. Novales Flamarique I 2016. Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones. Proc. R. Soc. B 283: 1826.20160058
     [Google Scholar]
  120. Novales Flamarique I 2018. Light exposure during embryonic and yolk-sac alevin development of Chinook salmon Oncorhynchus tshawytscha does not alter the spectral phenotype of photoreceptors. J. Fish Biol. 95:1214–21
     [Google Scholar]
  121. Nozawa M, Suzuki Y, Nei M 2009. Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. PNAS 106:166700–5
     [Google Scholar]
  122. Ogawa Y, Shiraki T, Asano Y, Muto A, Kawakami K et al. 2019. Six6 and Six7 coordinately regulate expression of middle-wavelength opsins in zebrafish. PNAS 116:104651–60
     [Google Scholar]
  123. Ohno S. 1970. Evolution by Gene Duplication Berlin/Heidelberg: Springer
  124. O'Quin KE, Hofmann CM, Hofmann HA, Carleton KL. 2010. Parallel evolution of opsin gene expression in African cichlid fishes. Mol. Biol. Evol. 27:122839–54
     [Google Scholar]
  125. Ott M. 2006. Visual accommodation in vertebrates: mechanisms, physiological response and stimuli. J. Comp. Physiol. A 192:297–111
     [Google Scholar]
  126. Owens GL, Rennison DJ, Allison WT, Taylor JS. 2012. In the four-eyed fish (Anableps anableps), the regions of the retina exposed to aquatic and aerial light do not express the same set of opsin genes. Biol. Lett. 8:186–89
     [Google Scholar]
  127. Palczewski K. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:5480739–45
     [Google Scholar]
  128. Patel JS, Brown CJ, Ytreberg FM, Stenkamp DL. 2018. Predicting peak spectral sensitivities of vertebrate cone visual pigments using atomistic molecular simulations. PLOS Comp. Biol. 14:1e1005974
     [Google Scholar]
  129. Phillips GAC, Carleton KL, Marshall NJ. 2016. Multiple genetic mechanisms contribute to visual sensitivity variation in the Labridae. Mol. Biol. Evol. 33:1201–15
     [Google Scholar]
  130. Pierce LX, Noche RR, Ponomareva O, Chang C, Liang JO. 2008. Novel functions for Period 3 and Exo-rhodopsin in rhythmic transcription and melatonin biosynthesis within the zebrafish pineal organ. Brain Res 1223:11–24
     [Google Scholar]
  131. Pignatelli V, Champ C, Marshall J, Vorobyev M. 2010. Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biol. Lett. 6:4537–39
     [Google Scholar]
  132. Porter ML, Roberts NW, Partridge JC. 2016. Evolution under pressure and the adaptation of visual pigment compressibility in deep-sea environments. Mol. Phylogenet. Evol. 105:160–65
     [Google Scholar]
  133. Raine JC, Hawryshyn CW. 2009. Changes in thyroid hormone reception precede SWS1 opsin downregulation in trout retina. J. Exp. Biol. 212:172781–88
     [Google Scholar]
  134. Randel N, Jékely G. 2016. Phototaxis and the origin of visual eyes. Philos. Trans. R. Soc. B 371:168520150042
     [Google Scholar]
  135. Rick IP, Bloemker D, Bakker TCM. 2012. Spectral composition and visual foraging in the three-spined stickleback (Gasterosteidae: Gasterosteus aculeatus L.): elucidating the role of ultraviolet wavelengths. Biol. J. Linn. Soc. 105:2359–68
     [Google Scholar]
  136. Roberts MR, Srinivas M, Forrest D, Morreale de Escobar G, Reh TA 2006. Making the gradient: Thyroid hormone regulates cone opsin expression in the developing mouse retina. PNAS 103:66218–23
     [Google Scholar]
  137. Sandkam BA, Campello L, O'Brien C, Nandamuri SP, Gammerdinger WJ et al. 2020. Tbx2a modulates switching of RH2 and LWS opsin gene expression. Mol. Biol. Evol. 37:72002–14
     [Google Scholar]
  138. Sandkam BA, Dalton B, Breden F, Carleton K. 2018. Reviewing guppy color vision: integrating the molecular and physiological variation in visual tuning of a classic system for sensory drive. Curr. Zool. 64:4535–45
     [Google Scholar]
  139. Sandkam BA, Joy JB, Watson CT, Breden F. 2017. Genomic environment impacts color vision evolution in a family with visually based sexual selection. Genome Biol. Evol. 9:113100–7
     [Google Scholar]
  140. Sanes JR, Masland RH. 2015. The types of retinal ganglion cells: current status and implications for neuronal classification. Annu. Rev. Neurosci. 38:221–46
     [Google Scholar]
  141. Savelli I, Novales Flamarique I, Iwanicki T, Taylor JS 2018. Parallel opsin switches in multiple cone types of the starry flounder retina: tuning visual pigment composition for a demersal life style. Sci. Rep. 8:4763
     [Google Scholar]
  142. Schultze M. 1866. Zur Anatomie und Physiologie der Retina [On the anatomy and physiology of the retina. ]. Arch. Mikrosk. Anat. 2:1175–286
     [Google Scholar]
  143. Schweikert LE, Fitak RR, Caves EM, Sutton TT, Johnsen S. 2018. Spectral sensitivity in ray-finned fishes: diversity, ecology and shared descent. J. Exp. Biol. 221:23jeb189761
     [Google Scholar]
  144. Schweikert LE, Caves EM, Solie SE, Sutton TT, Johnsen S. 2019. Variation in rod spectral sensitivity of fishes is best predicted by habitat and depth. J. Fish Biol. 95:1179–85
     [Google Scholar]
  145. Schweikert LE, Grace MS. 2018. Altered environmental light drives retinal change in the Atlantic tarpon (Megalops atlanticus) over timescales relevant to marine environmental disturbance. BMC Ecol 18:1
     [Google Scholar]
  146. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ et al. 2008. Speciation through sensory drive in cichlid fish. Nature 455:7213620–26
     [Google Scholar]
  147. Seiko T, Kishida T, Toyama M, Hariyama T, Okitsu T et al. 2020. Visual adaptation of opsin genes to the aquatic environment in sea snakes. BMC Evol. Biol. 20:158
     [Google Scholar]
  148. Shand J, Davies WL, Thomas N, Balmer L, Cowing JA et al. 2008. The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, Acanthopagrus butcheri. J. Exp. Biol. 211:91495–503
     [Google Scholar]
  149. Shimmura T, Nakayama T, Shinomiya A, Fukamachi S, Yasugi M et al. 2017. Dynamic plasticity in phototransduction regulates seasonal changes in color perception. Nat. Commun. 8:412
     [Google Scholar]
  150. Siebeck UE, Losey GS, Marshall J 2006. UV communication in fish. Communication in Fishes, Vol. 1 F Ladich, SP Collin, P Moller, BG Kapoor 423–56 Enfield, NH: Sci. Publ.
     [Google Scholar]
  151. Siebeck UE, Marshall NJ. 2001. Ocular media transmission of coral reef fish—can coral reef fish see ultraviolet light?. Vis. Res. 41:2133–49
     [Google Scholar]
  152. Siebeck UE, Marshall NJ. 2007. Potential ultraviolet vision in pre-settlement larvae and settled reef fish—a comparison across 23 families. Vis. Res. 47:172337–52
     [Google Scholar]
  153. Siebeck UE, Parker AN, Sprenger D, Mäthger LM, Wallis G 2010. A species of reef fish that uses ultraviolet patterns for covert face recognition. Curr. Biol. 20:5407–10
     [Google Scholar]
  154. Simões BF, Gower DJ, Rasmussen AR, Sarker MAR, Fry GC et al. 2020. Spectral diversification and trans-species allelic polymorphism during the land-to-sea transition in snakes. Curr. Biol. 30:132608–15.e4
     [Google Scholar]
  155. Smith EJ, Partridge JC, Parsons KN, White EM, Cuthill IC et al. 2002. Ultraviolet vision and mate choice in the guppy (Poecilia reticulata). Behav. Ecol. 13:111–19
     [Google Scholar]
  156. Spady TC, Parry JWL, 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. 23:81538–47
     [Google Scholar]
  157. Stieb SM, Carleton KL, Cortesi F, Marshall NJ, Salzburger W. 2016. Depth-dependent plasticity in opsin gene expression varies between damselfish (Pomacentridae) species. Mol. Ecol. 25:153645–61
     [Google Scholar]
  158. Stieb SM, Cortesi F, Sueess L, Carleton KL, Salzburger W, Marshall NJ. 2017. Why UV vision and red vision are important for damselfish (Pomacentridae): structural and expression variation in opsin genes. Mol. Ecol. 26:51323–42
     [Google Scholar]
  159. Stieb SM, de Busserolles F, Carleton KL, Cortesi F, Chung W-S et al. 2019. A detailed investigation of the visual system and visual ecology of the Barrier Reef anemonefish, Amphiprion akindynos. Sci. Rep 9:16459
     [Google Scholar]
  160. Stockman A, Sharpe LT. 2006. Into the twilight zone: the complexities of mesopic vision and luminous efficiency. Ophthalmic Physiol. Opt. 26:3225–39
     [Google Scholar]
  161. Sugawara T, Terai Y, Imai H, Turner GF, Koblmüller S et al. 2005. Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi. PNAS 102:155448–53
     [Google Scholar]
  162. Suzuki SC, Bleckert A, Williams PR, Takechi M, Kawamura S, Wong ROL 2013. Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. PNAS 110:3715109–14
     [Google Scholar]
  163. Taylor SM, Loew ER, Grace MS. 2011. Developmental shifts in functional morphology of the retina in Atlantic tarpon, Megalops atlanticus (Elopomorpha: Teleostei) between four ecologically distinct life-history stages. Vis. Neurosci. 28:4309–23
     [Google Scholar]
  164. Temple S, Hart NS, Marshall NJ, Collin SP 2010. A spitting image: specializations in archerfish eyes for vision at the interface between air and water. Proc. R. Soc. B 277: 1694.2607–15
     [Google Scholar]
  165. Terai Y, Miyagi R, Aibara M, Mizoiri S, Imai H et al. 2017. Visual adaptation in Lake Victoria cichlid fishes: depth-related variation of color and scotopic opsins in species from sand/mud bottoms. BMC Evol. Biol. 17:200
     [Google Scholar]
  166. Terai Y, Seehausen O, Sasaki T, Takahashi K, Mizoiri S et al. 2006. Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLOS Biol 4:12e433
     [Google Scholar]
  167. Tettamanti V, de Busserolles F, Lecchini D, Marshall NJ, Cortesi F. 2019. Visual system development of the spotted unicornfish, Naso brevirostris (Acanthuridae). J. Exp. Biol. 222:24jeb209916
     [Google Scholar]
  168. Thorpe A, Douglas RH. 1993. Spectral transmission and short-wave absorbing pigments in the fish lens—II. Effects of age. Vis. Res. 33:3301–7
     [Google Scholar]
  169. Thorpe A, Douglas RH, Truscott RJW. 1993. Spectral transmission and short-wave absorbing pigments in the fish lens—I. Phylogenetic distribution and identity. Vis. Res. 33:3289–300
     [Google Scholar]
  170. Torres-Dowdall J, Pierotti MER, Härer A, Karagic N, Woltering JM et al. 2017. Rapid and parallel adaptive evolution of the visual system of neotropical Midas cichlid fishes. Mol. Biol. Evol. 34:102469–85
     [Google Scholar]
  171. Tsujimura T. 2020. Mechanistic insights into the evolution of the differential expression of tandemly arrayed cone opsin genes in zebrafish. Dev. Growth Differ. 62:7–8465–75
     [Google Scholar]
  172. Valen R, Karlsen R, Helvik JV. 2018. Environmental, population and life-stage plasticity in the visual system of Atlantic cod. J. Exp. Biol. 221:1jeb165191
     [Google Scholar]
  173. Wald G. 1968. The molecular basis of visual excitation. Nature 219:5156800–7
     [Google Scholar]
  174. Ward MN, Churcher AM, Dick KJ, Laver CR, Owens GL et al. 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
     [Google Scholar]
  175. Weadick CJ, Loew ER, Rodd FH, Chang BSW 2012. Visual pigment molecular evolution in the Trinidadian pike cichlid (Crenicichla frenata): a less colorful world for neotropical cichlids?. Mol. Biol. Evol. 29:103045–60
     [Google Scholar]
  176. Wood P, Partridge JC. 1993. Opsin substitution induced in retinal rods of the eel (Anguilla anguilla (L.)): a model for G-protein-linked receptors. Proc. R. Soc. Lond. B 254: 1341.227–32
     [Google Scholar]
  177. Wright DS, Eijk R, Schuart L, Seehausen O, Groothuis TGG, Maan ME. 2020. Testing sensory drive speciation in cichlid fish: linking light conditions to opsin expression, opsin genotype and female mate preference. J. Evol. Biol. 33:4422–34
     [Google Scholar]
  178. Yokoyama S. 2008. Evolution of dim-light and color vision pigments. Annu. Rev. Genom. Hum. Genet. 9:259–82
     [Google Scholar]
  179. Yokoyama S, Jia H. 2020. Origin and adaptation of green-sensitive (RH2) pigments in vertebrates. FEBS Open Bio 10:5873–82
     [Google Scholar]
  180. Yokoyama S, Takenaka N. 2004. The molecular basis of adaptive evolution of squirrelfish rhodopsins. Mol. Biol. Evol. 21:112071–78
     [Google Scholar]
  181. Yoshimatsu T, Schröder C, Nevala NE, Berens P, Baden T. 2020. Fovea-like photoreceptor specializations underlie single UV cone driven prey-capture behavior in zebrafish. Neuron 107:2320–37
     [Google Scholar]
  182. Zhang H, Futami K, Horie N, Okamura A, Utoh T et al. 2000. Molecular cloning of fresh water and deep-sea rod opsin genes from Japanese eel Anguilla japonica and expressional analyses during sexual maturation. FEBS Lett 469:139–43
     [Google Scholar]
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The Visual Opsin Gene Repertoires of Teleost Fishes: Evolution, Ecology, and Function
Annual Review of Cell and Developmental Biology 37, 441 (2021); https://doi.org/10.1146/annurev-cellbio-120219-024915
/content/journals/10.1146/annurev-cellbio-120219-024915
/content/journals/10.1146/annurev-cellbio-120219-024915
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