Diversity of color vision: Not all Australian marsupials are trichromatic

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Ebeling, Wiebke ^b   Natoli, Riccardo C ^a   Hemmi, Jan M ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF TASMANIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN; SCOTOPSIN; VISUAL PIGMENT; ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUSTRALIA; COLOR VISION; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MARSUPIAL; MICROSPECTROPHOTOMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RETINA CONE; SPECIES DIFFERENCE; ANIMAL; ANTIBODY SPECIFICITY; GENETICS; IMAGE PROCESSING; METABOLISM; METHODOLOGY; PHYSIOLOGY; RETINA; X CHROMOSOME;

MACROPUS EUGENII; MAMMALIA; METATHERIA; PRIMATES; SETONIX BRACHYURUS; SMINTHOPSIS; SMINTHOPSIS CRASSICAUDATA; TARSIPEDIDAE;

ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; AUSTRALIA; COLOR VISION; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MACROPODIDAE; MALE; MARSUPIALIA; OPSINS; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; X CHROMOSOME;

EID: 78650083529     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014231     Document Type: Article

References (62)

1. Ahnelt PK, Kolb H (2000) The mammalian photoreceptor mosaic-adaptive design. Progr Ret Eye Res 19: 711-777.
2. Ebrey T, Koutalos Y (2001) Vertebrate Photoreceptors. Progr Ret Eye Res 20: 49-94.
3. Jacobs GH (2009) Evolution of colour vision in mammals. Proc R Soc Lond B 34: 2957-2967. (DOI: 10.1098/rstb.2009.0039).
4. Fasick JI, Cronin TW, Hunt DM, Robinson PR (1998) The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci 15: 643-651.
5. Peichl L, Behrmann G, Kröger RHH (2001) For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Europ J Neurosci 13: 1520-1528.
6. Levenson DH, Ponganis PJ, Crognale MA, Deegan JF II, Dizon A, et al. (2006) Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter. J Comp Physiol A 192: 833-843. (DOI: 10.1007/s00359-006-0121-x).
7. Dulai KS, von Dornum M, Mollon JD, Hunt DM (1999) The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res 9: 629-638. (DOI: 10.1101/gr.9.7.629).
8. Mollon JD, Bowmaker JK, Jacobs GH (1984) Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proc R Soc Lond B 222: 373-399.
9. Jacobs GH, Deegan JF II, Neitz J, Crognale MA, Neitz M (1993) Photopigments and color vision in the nocturnal monkey, Aotus. Vision Res 33: 1773- 1783.
10. Kawamura S, Kubotera N (2003) Ancestral loss of short wave-sensitive cone visual pigment in lorisiform prosimians, contrasting with its strict conservation in other prosimians. J Mol Evol 58: 314-321. (DOI: 10.1007/s00239-003-2553-z).
11. Müller B, Goodman S, Peichl L (2007) Cone photoreceptor diversity in the retinas of fruit bats (Megachiroptera). Brain Behav Evol 70: 90-104. (DOI:10.1159/000102971).
12. Müller B, Glösmann M, Peichl L, Knop GC, Hagemann C, et al. (2009) Bat eyes have ultraviolet-sensitive cone photoreceptors. PLoS ONE 4: e6390. (DOI:10.1371/journal.pone.0006390).
13. Wang D, Oakley T, Mower J, Shimmin LC, Yim S, et al. (2004) Molecular evolution of bat color vision genes. Mol Biol Evol 21: 295-302. (DOI: 10.1093/ molbev/msh015).
14. Winter Y, López J, von Helversen O (2003) Ultraviolet vision in a bat. Nature 425: 612-614. (DOI: 10.1038/nature01971).
15. Zhao H, Rossiter SJ, Teeling EC, Li C, Cotton JA, et al. (2009) The evolution of color vision in nocturnal mammals. Proc Natl Acad Sci U S A 106: 8980-8985. (DOI: 10.1073_pnas.0813201106).
16. Davies WL, Carvalho LS, Cowing JA, Beazley LD, Hunt DM, et al. (2007) Visual pigments of the platypus: a novel route to mammalian colour vision. Curr Biol 17: R161-R163.
17. Wakefield MJ, Anderson M, Chang E, Wei K-J, Kaul R, et al. (2008) Cone visual pigments of monotremes: filling the phylogenetic gap. Vis Neurosci 25: 257-264. (DOI: 10.10170S0952523808080255).
18. Hemmi JM (1999) Dichromatic colour vision in an Australian marsupial, the tammar wallaby. J Comp Physiol A 185: 509-515.
19. Hemmi JM, Grünert U (1999) Distribution of photoreceptor types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Vis Neurosci 16: 291-302.
20. Deeb SS, Wakefield MJ, Tada T, Marotte L, Yokoyama S, et al. (2003) The cone visual pigments of an Australian marsupial, the tammar wallaby (Macropus eugenii): sequence, spectral tuning, and evolution. Mol Biol Evol 20: 1642-1649. (DOI: 10.1093/molbev/msg181).
21. Wikler KC, Rakic P (1990) Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. J Neurosci 10: 3390-3401.
22. Ahnelt PK, Hokoç JN, Röhlich P (1995) Photoreceptors in a primitive mammal, the South American opossum, Didelphis marsupialis aurita: characterization with anti-opsin immunolabeling. Vis Neurosci 12: 793-804.
23. Hunt DM, Chan J, Carvalho LS, Hokoc JN, Ferguson MC, et al. (2009) Cone visual pigments in two species of South American marsupials. Gene 433: 50-55. (DOI: 10.1016/j.gene.2008.12.006).
24. Jacobs GH, Williams GA (2010) Cone pigments in a North American marsupial, the opossum (Didelphis virginiana). J Comp Physiol A 196: 379-384. (DOI:10.1007/s00359-010-0519-3).
25. Palacios AG, Bozinovic F, Vielma A, Arrese CA, Hunt DM, et al. (2010) Retinal photoreceptor arrangement, SWS1 and LWS opsin sequence, and electroretinography in the South American marsupial Thylamys elegans (Waterhouse, 1839). J Comp Neurol 518: 1589-1602. (DOI: 10.1002/cne.22292).
26. Hunt DM, Carvalho LS, Cowing JA, Davies WL (2009) Evolution and spectral tuning of visual pigments in birds and mammals. Proc R Soc Lond B 364: 2941-2955. (DOI: 10.1098/rstb.2009.0044).
27. Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2002) Trichromacy in Australian marsupials. Curr Biol 12: 657-660.
28. Arrese CA, Oddy AY, Runham PB, Hart NS, Shand J, et al. (2005) Cone topography and spectral sensitivity in two potentially trichromatic marsupials, the quokka (Setonix brachyurus) and quenda (Isoodon obesulus). Proc R Soc Lond B 272: 791-796. (DOI: 10.1098/rspb.2004.3009).
29. Arrese CA, Rodger J, Beazley LD, Shand J (2003) Topographies of retinal cone photoreceptors in two Australian marsupials. Vis Neurosci 20: 307-311. (DOI:10.10170S0952523803203096).
30. Arrese CA, Beazley LD, Neumeyer C (2006) Behavioural evidence for marsupial trichromacy. Curr Biol 16: R193-R194.
31. Strachan J, Chang L-YE, Wakefield MJ, Marshall Graves JA, Deeb SS (2004) Cone visual pigments of the Australian marsupials, the stripe-faced and fat-tailed dunnarts: sequence and inferred spectral properties. Vis Neurosci 21: 223-229. (DOI: 10.10170S0952523804213281).
32. Cowing JA, Arrese CA, Davies WL, Beazley LD, Hunt DM (2008) Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus). Proc R Soc Lond B 275: 1491-1499. (DOI: 10.1098/rspb.2008.0248).
33. Hicks D, Barnstable CJ (1987) Different rhodopsin monoclonal antibodies reveal different binding patterns on developing and adult rat retina. J Histochem Cytochem 35: 1317-1328.
34. Wang Y, Macke JP, Merbs SL, Zack DJ, Klaunberg B, et al. (1992) A locus control region adjacent to the human red and green visual pigment genes. Neuron 9: 429-440.
35. Arrese C, Dunlop SA, Harman AM, Braekevelt CR, Ross WM, et al. (1999) Retinal structure and visual acuity in a polyprotodont marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Brain Behav Evol 53: 111-126. (DOI:10.1159/000006588).
36. Schoenenberger P, Grunditz Å, Rose T, Oertner TG (2008) Optimizing the spatial resolution of Channelrhodopsin-2 activation. Brain Cell Biol 36: 119-127.
37. Oddy AY, Ager EI, Cowing J, Rodger J, Hunt DM (2003) Direct submission to GenBank, accession number AY159786.
38. Hunt DM, Arrese CA, von Dornum M, Rodger J, Oddy A, et al. (2003) The rod opsin pigments from two marsupial species, the South American bare-tailed woolly opossum and the Australian fat-tailed dunnart. Gene 323: 157-162. (DOI: 10.1016/j.gene.2003.09.016).
39. Xiao M, Hendrickson A (2000) Spatial and temporal expression of short, long/ medium, or both opsins in human fetal cones. J Comp Neurol 425: 545-559.
40. Applebury ML (2001) Response: the uncommon retina of the common house mouse. Trends Neurosci 24: 250.
41. Glösmann M, Ahnelt PK (2002) A mouse-like retinal cone phenotype in the Syrian hamster: S opsin coexpressed with M opsin in a common cone photoreceptor. Brain Res 929: 139-146.
42. Gamlin PDR, McDougal DH, Pokorny J, Smith VC, Yau K-W, et al. (2007) Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res 47: 946-954. (DOI: 10.1016/j.visres.2006.12.015).
43. Dkhissi-Benyahya O, Rieux C, Hut RA, Cooper HM (2006) Immunohistochemical evidence of a melanopsin cone in human retina. Invest Ophthalmol Vis Sci 74: 1636-1641. (DOI: 10.1167/iovs.05-1459).
44. Pires SP, Shand J, Bellingham J, Arrese C, Turton M, et al. (2007) Isolation and characterization of melanopsin (Opn4) from the Australian marsupial Sminthopsis crassicaudata. Proc R Soc Lond B 274: 2791-2799.
45. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Progr Ret Eye Res 19: 385-419.
46. Collin SP, Knight MA, Davies WL, Potter IC, Hunt DM, et al. (2003) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13: R864-R865.
47. Liebman PA, Entine G (1968) Visual pigments of frog and tadpole (Rana pipiens). Vision Res 8: 761-775.
48. McDevitt DS, Brahma SK, Jeanny J-C, Hicks D (1993) Presence and foveal enrichment of rod opsin in the "all cone" retina of the American chameleon. Anat Rec 237: 299-307.
49. Raymond PA, Barthel LK, Rounsife ME, Sullivan SA, Knight JK (1993) Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cone. Neuron 10: 1161-1174.
50. Ma J-X, Znoiko S, Othersen KL, Ryan JC, Das J, et al. (2001) A visual pigment expressed in both rod and cone photoreceptors. Neuron 32: 451-461.
51. Bennis M, Molday RS, Versaux-Botteri C, Repérant J, Jeanny J-C, et al. (2005) Rhodopsin-like immunoreactivity in the 'all cone' retina of the chameleon (Chameleo chameleo). Exp Eye Res 80: 623-627. (DOI: 10.1016/j.exer. 2004.11.004).
52. Molday RS, MacKenzie D (1983) Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry 22: 653-660. (DOI: 10.1021/bi00272a020).
53. Andreadis A, Gallego ME, Nadal-Ginard B (1987) Generation of protein isoform diversity by alternative splicing: mechanistic and biological implications. Ann Rev Cell Biol 3: 207-242.
54. Granneman JG, Zhai Y, Zhu Z, Bannon MJ, Burchett SA, et al. (1998) Molecular characterization of human and rat RGS 9L, a novel splice variant enriched in dopamine target regions, and chromosomal localization of the RGS 9 gene. Mol Pharmacol 54: 687-694.
55. Jiang M, Shen D, Tao L, Pandey S, Heller K, et al. (1995) Alternative splicing in human retinal mRNS transcripts of an opsin-related protein. Exp Eye Res 60: 401-406.
56. Hoffmann M, Tripathi N, Henz SR, Lindholm AK, Weigel D, et al. (2007) Opsin gene duplication and diversification in the guppy, a model for sexual selection. Proc R Soc Lond B 274: 33-42. (DOI: 10.1098/rspb.2006.3707).
57. Jacobs GH, Neitz J, Deegan JF II (1991) Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353: 655-666.
58. Jacobs GH, Williams GA, Fenwick JA (2004) Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Res 44: 1615-1622. (DOI: 10.1016/j.visres.2004.01.016).
59. Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263: 593-599.
60. De Araújo MFP, Lima EM, Pessoa VF (2006) Modeling dichromatic and trichromatic sensitivity to the color properties of fruits eaten by squirrel monkeys (Saimiri sciureus). Am J Primatol 68: 1129-1137. (DOI: 10.1002/ajp.20312).
61. Sumner P, Arrese CA, Partridge JC (2005) The ecology of visual pigment tuning in an Australian marsupial: the honey possum Tarsipes rostratus. J Exp Biol 208: 1803-1815. (DOI: 10.1242/jeb.01610).
62. Nilsson MA, Arnason U, Spencer PBS, Janke A (2004) Marsupial relationships and a timeline for marsupial radiation in South Gondwana. Gene 340: 189-196. (DOI: 10.1016/j.gene.2004.07.040).