• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Aug 2001; 158(4): 1697–1710.
PMCID: PMC1461741

The molecular genetics and evolution of red and green color vision in vertebrates.

Abstract

To better understand the evolution of red-green color vision in vertebrates, we inferred the amino acid sequences of the ancestral pigments of 11 selected visual pigments: the LWS pigments of cave fish (Astyanax fasciatus), frog (Xenopus laevis), chicken (Gallus gallus), chameleon (Anolis carolinensis), goat (Capra hircus), and human (Homo sapiens);and the MWS pigments of cave fish, gecko (Gekko gekko), mouse (Mus musculus), squirrel (Sciurus carolinensis), and human. We constructed these ancestral pigments by introducing the necessary mutations into contemporary pigments and evaluated their absorption spectra using an in vitro assay. The results show that the common ancestor of vertebrates and most other ancestors had LWS pigments. Multiple regression analyses of ancestral and contemporary MWS and LWS pigments show that single mutations S180A, H197Y, Y277F, T285A, A308S, and double mutations S180A/H197Y shift the lambda(max) of the pigments by -7, -28, -8, -15, -27, and 11 nm, respectively. It is most likely that this "five-sites" rule is the molecular basis of spectral tuning in the MWS and LWS pigments during vertebrate evolution.

Full Text

The Full Text of this article is available as a PDF (248K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Yokoyama S, Radlwimmer FB. The "five-sites" rule and the evolution of red and green color vision in mammals. Mol Biol Evol. 1998 May;15(5):560–567. [PubMed]
  • Asenjo AB, Rim J, Oprian DD. Molecular determinants of human red/green color discrimination. Neuron. 1994 May;12(5):1131–1138. [PubMed]
  • Besharse JC, Witkovsky P. Light-evoked contraction of red absorbing cones in the Xenopus retina is maximally sensitive to green light. Vis Neurosci. 1992 Mar;8(3):243–249. [PubMed]
  • Merbs SL, Nathans J. Role of hydroxyl-bearing amino acids in differentially tuning the absorption spectra of the human red and green cone pigments. Photochem Photobiol. 1993 Nov;58(5):706–710. [PubMed]
  • Bowmaker JK, Heath LA, Wilkie SE, Hunt DM. Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res. 1997 Aug;37(16):2183–2194. [PubMed]
  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ. Molecular phylogenetics and the origins of placental mammals. Nature. 2001 Feb 1;409(6820):614–618. [PubMed]
  • Chan T, Lee M, Sakmar TP. Introduction of hydroxyl-bearing amino acids causes bathochromic spectral shifts in rhodopsin. Amino acid substitutions responsible for red-green color pigment spectral tuning. J Biol Chem. 1992 May 15;267(14):9478–9480. [PubMed]
  • Nei M, Zhang J, Yokoyama S. Color vision of ancestral organisms of higher primates. Mol Biol Evol. 1997 Jun;14(6):611–618. [PubMed]
  • Neitz M, Neitz J, Jacobs GH. Spectral tuning of pigments underlying red-green color vision. Science. 1991 May 17;252(5008):971–974. [PubMed]
  • Novacek MJ. Mammalian phylogeny: shaking the tree. Nature. 1992 Mar 12;356(6365):121–125. [PubMed]
  • Okano T, Fukada Y, Artamonov ID, Yoshizawa T. Purification of cone visual pigments from chicken retina. Biochemistry. 1989 Oct 31;28(22):8848–8856. [PubMed]
  • David-Gray ZK, Cooper HM, Janssen JW, Nevo E, Foster RG. Spectral tuning of a circadian photopigment in a subterranean 'blind' mammal (Spalax ehrenbergi). FEBS Lett. 1999 Nov 19;461(3):343–347. [PubMed]
  • Oprian DD, Asenjo AB, Lee N, Pelletier SL. Design, chemical synthesis, and expression of genes for the three human color vision pigments. Biochemistry. 1991 Dec 3;30(48):11367–11372. [PubMed]
  • Palacios AG, Varela FJ, Srivastava R, Goldsmith TH. Spectral sensitivity of cones in the goldfish, Carassius auratus. Vision Res. 1998 Jul;38(14):2135–2146. [PubMed]
  • Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, et al. Crystal structure of rhodopsin: A G protein-coupled receptor. Science. 2000 Aug 4;289(5480):739–745. [PubMed]
  • Ebrey T, Koutalos Y. Vertebrate photoreceptors. Prog Retin Eye Res. 2001 Jan;20(1):49–94. [PubMed]
  • Radlwimmer FB, Yokoyama S. Cloning and expression of the red visual pigment gene of goat (Capra hircus). Gene. 1997 Oct 1;198(1-2):211–215. [PubMed]
  • Fasick JI, Cronin TW, Hunt DM, Robinson PR. The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci. 1998 Jul-Aug;15(4):643–651. [PubMed]
  • Radlwimmer FB, Yokoyama S. Genetic analyses of the green visual pigments of rabbit (Oryctolagus cuniculus) and rat (Rattus norvegicus). Gene. 1998 Sep 18;218(1-2):103–109. [PubMed]
  • Hadjeb N, Berkowitz GA. Preparation of T-over-hang vectors with high PCR product cloning efficiency. Biotechniques. 1996 Jan;20(1):20–22. [PubMed]
  • Shoshani J, McKenna MC. Higher taxonomic relationships among extant mammals based on morphology, with selected comparisons of results from molecular data. Mol Phylogenet Evol. 1998 Jun;9(3):572–584. [PubMed]
  • Hubbard R, Kropf A. THE ACTION OF LIGHT ON RHODOPSIN. Proc Natl Acad Sci U S A. 1958 Feb;44(2):130–139. [PMC free article] [PubMed]
  • Huchon D, Catzeflis FM, Douzery EJ. Molecular evolution of the nuclear von Willebrand factor gene in mammals and the phylogeny of rodents. Mol Biol Evol. 1999 May;16(5):577–589. [PubMed]
  • Jacobs GH. The distribution and nature of colour vision among the mammals. Biol Rev Camb Philos Soc. 1993 Aug;68(3):413–471. [PubMed]
  • Sun H, Macke JP, Nathans J. Mechanisms of spectral tuning in the mouse green cone pigment. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8860–8865. [PMC free article] [PubMed]
  • Johnson RL, Grant KB, Zankel TC, Boehm MF, Merbs SL, Nathans J, Nakanishi K. Cloning and expression of goldfish opsin sequences. Biochemistry. 1993 Jan 12;32(1):208–214. [PubMed]
  • Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992 Jun;8(3):275–282. [PubMed]
  • Waddell PJ, Cao Y, Hauf J, Hasegawa M. Using novel phylogenetic methods to evaluate mammalian mtDNA, including amino acid-invariant sites-LogDet plus site stripping, to detect internal conflicts in the data, with special reference to the positions of hedgehog, armadillo, and elephant. Syst Biol. 1999 Mar;48(1):31–53. [PubMed]
  • Kawamura S, Yokoyama S. Functional characterization of visual and nonvisual pigments of American chameleon (Anolis carolinensis). Vision Res. 1998 Jan;38(1):37–44. [PubMed]
  • Kawamura S, Blow NS, Yokoyama S. Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics. 1999 Dec;153(4):1839–1850. [PMC free article] [PubMed]
  • Waddell PJ, Cao Y, Hasegawa M, Mindell DP. Assessing the Cretaceous superordinal divergence times within birds and placental mammals by using whole mitochondrial protein sequences and an extended statistical framework. Syst Biol. 1999 Mar;48(1):119–137. [PubMed]
  • Khorana HG, Knox BE, Nasi E, Swanson R, Thompson DA. Expression of a bovine rhodopsin gene in Xenopus oocytes: demonstration of light-dependent ionic currents. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7917–7921. [PMC free article] [PubMed]
  • Kleinschmidt J, Harosi FI. Anion sensitivity and spectral tuning of cone visual pigments in situ. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9181–9185. [PMC free article] [PubMed]
  • Kumar S, Hedges SB. A molecular timescale for vertebrate evolution. Nature. 1998 Apr 30;392(6679):917–920. [PubMed]
  • Winderickx J, Lindsey DT, Sanocki E, Teller DY, Motulsky AG, Deeb SS. Polymorphism in red photopigment underlies variation in colour matching. Nature. 1992 Apr 2;356(6368):431–433. [PubMed]
  • Witkovsky P, Levine JS, Engbretson GA, Hassin G, MacNichol EF., Jr A microspectrophotometric study of normal and artificial visual pigments in the photoreceptors of Xenopus laevis. Vision Res. 1981;21(6):867–873. [PubMed]
  • Madsen O, Scally M, Douady CJ, Kao DJ, DeBry RW, Adkins R, Amrine HM, Stanhope MJ, de Jong WW, Springer MS. Parallel adaptive radiations in two major clades of placental mammals. Nature. 2001 Feb 1;409(6820):610–614. [PubMed]
  • Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997 Oct;13(5):555–556. [PubMed]
  • Merbs SL, Nathans J. Absorption spectra of human cone pigments. Nature. 1992 Apr 2;356(6368):433–435. [PubMed]
  • Yang Z, Kumar S, Nei M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics. 1995 Dec;141(4):1641–1650. [PMC free article] [PubMed]
  • Yokoyama R, Yokoyama S. Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9315–9318. [PMC free article] [PubMed]
  • Yokoyama R, Knox BE, Yokoyama S. Rhodopsin from the fish, Astyanax: role of tyrosine 261 in the red shift. Invest Ophthalmol Vis Sci. 1995 Apr;36(5):939–945. [PubMed]
  • Yokoyama S. Molecular bases of color vision in vertebrates. Genes Genet Syst. 1999 Oct;74(5):189–199. [PubMed]
  • Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res. 2000 Jul;19(4):385–419. [PubMed]
  • Yokoyama S. Phylogenetic analysis and experimental approaches to study color vision in vertebrates. Methods Enzymol. 2000;315:312–325. [PubMed]
  • Yokoyama S, Radlwimmer FB. The "five-sites" rule and the evolution of red and green color vision in mammals. Mol Biol Evol. 1998 May;15(5):560–567. [PubMed]
  • Yokoyama S, Radlwimmer FB. The molecular genetics of red and green color vision in mammals. Genetics. 1999 Oct;153(2):919–932. [PMC free article] [PubMed]
  • Yokoyama S, Yokoyama R. Molecular evolution of human visual pigment genes. Mol Biol Evol. 1989 Mar;6(2):186–197. [PubMed]
  • Yokoyama S, Blow NS, Radlwimmer FB. Molecular evolution of color vision of zebra finch. Gene. 2000 Dec 23;259(1-2):17–24. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...