Identification and characterization of visual pigments in caecilians (Amphibia: Gymnophiona), an order of limbless vertebrates with rudimentary eyes

Journal of Experimental Biology

Volumn 213, Issue 20, 2010, Pages 3586-3592

  Mohun, S M ^a,b   Davies, W L ^a,c   Bowmaker, J K ^a   Pisani, D ^d   Himstedt, W ^e   Gower, D J ^b   Hunt, D M ^a,f   Wilkinson, M ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^e DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Caecilian; Evolution; Gymnophiona; Opsin; Spectral tuning; Visual pigments

Indexed keywords

SCOTOPSIN; VISUAL PIGMENT;

AMPHIBIA; ANIMAL; ARTICLE; BAYES THEOREM; CHEMISTRY; EYE; GENETICS; LIMB; METABOLISM; MICROSPECTROPHOTOMETRY; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ANALYSIS;

AMPHIBIANS; ANIMALS; BAYES THEOREM; CONSERVED SEQUENCE; EXTREMITIES; EYE; MICROSPECTROPHOTOMETRY; PHYLOGENY; RETINAL PIGMENTS; ROD OPSINS; SEQUENCE ANALYSIS, PROTEIN;

AMPHIBIA; ANURA; CAECILIA; CAUDATA; GEOTRYPETES SERAPHINI; GYMNOPHIONA; ICHTHYOPHIS KOHTAOENSIS; RHINATREMA BIVITTATUM; SALAMANDROIDEA; TYPHLONECTES NATANS; VERTEBRATA;

EID: 77957841228     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.045914     Document Type: Article

References (55)

1. Ala-Laurila, P., Saarinen, P., Albert, R., Koskelainen, A. and Donner. K. (2002). Temperature effects on spectral properties of red and green rods in toad retina. Vis. Neurosci. 19, 781-792.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Bowmaker, J. K. and Hunt, D. M. (2006). Evolution of vertebrate visual pigments Curr. Biol. 16, R484-R489.
4. Bowmaker, J. K., Govardovskii, V. I., Shukolyukov, S. A., Zueva, L. V., Hunt, D. M., Sideleva, V. G. and Smirnova, O. G. (1994). Visual pigments and the photic environment: the cottoid fish of Lake Baikal. Vis. Res. 34, 591-605.
5. Burger, R. M., Boylan, J. and Aucone, B. M. (2007). The effects of phototaxis and thigmotaxis on microhabitat selection by a caecilian amphibian (genus Ichthyophis) Herpetol. J. 17 19-23.
6. Chen, N., Ma, J. X., Corson, D. W., Hazard, E. S. and Crouch, R. K. (1996). Molecular cloning of a rhodopsin gene from salamander rods. Invest. Ophthalmol. Vis. Sci. 37 1907-1913.
7. Crescitelli, F. (1972). The visual cells and visual pigments of the vertebrate eye Photochemistry of Vision: Handbook of Sensory Physiology (ed. H. J. A. Dartnall), pp. 245-363. Berlin: Springer.
8. Davies, W. L., Cowing, J. A., Carvalho, L. S., Potter, I. C., Tresize, A. E. O., Hunt, D. M. and Collin, S. P. (2007a). Functional characterization tuning and regulation of visual pigment gene expression in an anadromous lamprey. FASEBJ. 21 2713-2724.
9. Davies, W. L., Carvalho, L. S., Cowing, J. A., Beazley, L. D., Hunt, D. M. and Arrese, C. A. (2007b). Visual pigments of the platypus: a novel route to mammalian colour vision. Curr. Biol. 17, 161-162.
10. Davies, W. L., Carvalho, L. S., Tay, B., Brenner, S., Hunt, D. M. and Venkatesh, B. (2009). Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Gen. Res. 19, 415-426.
11. Endler, J. A. (1993). The color of light in forests and its implications. Ecol. Monogr. 63, 1-27.
12. Fasick, J. I. and Robinson, P. R. (2000). Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth. Vis. Neurosci. 17, 781-788.
13. Fasick, J. I., Cronin, T. W., Hunt, D. M. and Robinson, P. R. (1998). The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis. Neurosci. 15 643-651.
14. Foster, R. G., Garcia Fernandez, J. M., Provencio, I. and Degrip, W. J. (1993). Opsin localisation and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J. Comp. Physiol. A 172, 33-45.
15. Franke, R. R., Sakmar, T. P., Oprian, D. D. and Khorana, H. G. (1988). A single amino acid substitution in rhodopsin (Lys248Leu) prevents activation of transducin. J. Biol. Chem. 263 2119-2122.
16. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sa, R. O., Channing, A., Wilkinson, M., Donnellan, S. C. et al. (2006). The amphibian tree of life. Bull. Am. Mus. Nat. Hist. 297, 1-370.
17. Fyhrquist, N., Donner, K., Hargrave, P. A., Mcdowell, J. H., Popp, M. P. and Smith, W. C. (1998). Rhodopsins from three frog and toad species: sequences and functional comparisons. Exp. Eye Res. 66 295-305.
18. Govardovskii, V. I., Fyhrquist, N., Reuter, T., Kuzmin, D. G. and Donner, K. (2000). In search of the visual pigment template. Vis. Neurosci. 17, 509-528.
19. Gower, D. J., Loader, S. P., Wilkinson, M. and Moncreiff, C. B. (2004). Niche separation and comparative abundance of Boulengerula boulengeriand Scolecomorphus vittatus (Amphibia: Gymnophiona) in East Usambara forest, Tanzania. Afr. J. Herpetol. 53, 183-190.
20. Harosi, F. (1975). Absorption spectra and linear dichroism of some amphibianphotoreceptors J. Gen. Physiol. 66, 357-382.
21. Hart, N. S. and Hunt, D. M. (2007). Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat. 169, S7-S26.
22. Henikoff, S. and Henikoff, J. G. (1992). Amino acid substitution matrices from protein blocks. Proc. Nalt. Acad. Sci. 89, 10915-10919.
23. Himstedt, W. (1995). Structure and function of the eyes in the caecilian Ichthyophis kohtaoensis (Amphibia, Gymnophiona) Zoo. Anal. Comp. Syst. 99, 81-94.
24. Himstedt, W. (1996). Die Blindwuhlen. Neue Brehm-Bucherei Vol. 630. Magdeburg/Heidelberg: Westarp/Spektrum.
25. Himstedt, W. and Simon, D. (1995). Sensory basis of foraging behaviour in caecilians (Amphibia, Gymnophiona) Herp. J. 5, 266-270.
26. Hope, A. J., Partridge, J. C., Dulai, K. S. and Hunt, D. M. (1997). Mechanisms of wavelength tuning in the rod opsins of deep-sea fishes Proc. R. Soc. Lond. B. Biol. Sci. 264 155-163.
27. Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754-755.
28. Hunt, D. M., Fitzgibbon, J., Slobodyanyuk, S. J. and Bowmaker, J. K. (1996). Spectral tuning and molecular evolution of rod visual pigments in the species flock of cottoid fish in Lake Baikal. Vision Res.36 1217-1224.
29. Hunt, D. M., Wilkie, S. E., Bowmaker, J. K. and Poopalasundaram, S. (2001a). Vision in the ultraviolet Cell. Mol. Life Sci. 58 1583-1598.
30. Hunt, D. M., Dulai, K. S., Partridge, J. C., Cottrill, P. and Bowmaker, J. K. (2001b). The molecular basis for spectral tuning of rod visual pigments in deep-sea fish. J. Exp. Biol. 204, 3333-3344.
31. Jones, D. T., Loader, S. P. and Gower, D. J. (2006). Trophic ecology of East African caecilians (Amphibia: Gymnophiona), and their impact on forest soil invertebrates J. Zool. 269 117-126.
32. Kos, M., Bulog, B., Szel, A. and Rohlich, P. (2001). Immunocytochemical demonstration of visual pigments in the degenerate retinal and pineal photoreceptors of the blind cave salamander (Proteus anguinus). Cell Tissue Res. 303, 15-25.
33. Kupfer, A., Nabhitabhata, J. and Himstedt, W. (2004). Reproductive ecology of female caecilian amphibians (genus Ichthyophis): a baseline study. Biol. J. Linn. Soc. Lond. 83, 207-217.
34. Liebman, P. A. and Entine, G. (1968). Visual pigments of frog and tadpole (Rana pipiens). Vis. Res. 8, 761-775.
35. Lythgoe, J. N. (1979). The Ecology of Vision .Oxford: Clarendon.
36. Maddison, D. R. and Maddison, W. P. (2000). Macclade Version 4, Analysis of Phylogeny and Character Evolution. Sunderland, MA: Sinauer Associates.
37. Munz, F. W. and McFarland, W. N. (1977). Evolutionary adaptations of fishes to the photic environment The Visual System of Vertebrates (ed. F. Crescitelli), pp. 194-274. New York: Springer.
38. New York: Springer-Verlag. Nguyen, B. (2003). Sind Blindwuehlen blind? Histologische und immunhistochemische Untersuchungen an den Augen von Gymnophionen. PhD thesis University of Technology, Darmstadt, Germany.
39. Norris, H. P. and Hughes, S. P. (1918). The cranial and anterior spinal nerves of the caecilian amphibians. J. Morphol. 31, 490-557.
40. Partridge, J. C., Speare, P., Shand, J., Muntz, W. R. and Williams, D. M. (1992). Microspectrophotometric determinations of rod visual pigments in some adult and larval Australian amphibians. Vis. Neurosci. 9 137-142.
41. Peichl, L. (2005). Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287A, 1001-1012.
42. Roelants, K., Gower, D. J., Wilkinson, M., Loader, S. P., Biju, S. D., Guillaume, K., Moriau, L. and Bossuyt, F. (2007). Global patterns of diversification in the history of modern amphibians. Proc. Natl. Acad. Sci. USA 104, 887-892.
43. Rohlich, P. and Szel, A. (2000). Photoreceptor cells in the Xenopus retina. Microsc. Res. Tech. 50 327-337.
44. Ronquist, F. and Huelsenbeck, J. P. (2003). MRBAYES 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
45. Sakakibara, S., Hiramatsu, H., Takahashi, Y., Hisatomi, O., Kobayashi, Y., Sakami, S., Saito, T. and Tokunaga, F. (2002). Opsin expression in adult, developing, and regenerating newt retinas Mol. Brain Res. 103, 28-35.
46. San Mauro, D. (2010). A multilocus timescale for the origin of extant amphibians. Mol. Phylogenet. Evol. 56, 554-561.
47. Takahashi, Y., Hisatomi, O., Sakakibara, S., Tsukahara, Y., Ebrey, T. G. and Tokunaga, F. (2001). Molecular cloning of the blue-sensitive opsin expressed In the Japanese common newt (Cynopspyrrhogaster). Invest Ophthalmol. Vis. Sci. 42, 984.
48. Taylor, E. H. (1968). The Caecilians of the World: a Taxonomic Analysis. Lawrence, KS: University of Kansas Press.
49. Trontelj, P., Goricki, S., Polak, S., Verovnik, R., ZakSek, V. and Sket, B. (2007). Age estimates for some subterranean taxa and lineages in the Dinaric Karst. Acta Carsologica 36 183-189.
50. Venkatesh, B., Erdmann, M. V. and Brenner, S. (2001). Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proc. Natl. Acad. Sci, USA 98, 11382-11387.
51. Wake, M. H. (1980). Morphological Information on caeclllan eye function. Am. Zool. 20. 785.
52. Wake, M. H. (1985). The comparative morphology and evolution of the eyes of caecilians (Amphibia; Gymnophiona. Zoomorphologyy 105. 277-295.
53. Walls, G. (1942). The Vertebrate Eye and its Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Institute of Science, Bull 19.
54. Wilkinson, M. and Nussbaum, R. A. (2006). Caecilian phylogeny and classification. In Reproductive Biology and Phylogeny of Gymnophiona (Caecilians) (ed. Exbrayet). pp. 39-78. Enfield: Science Publishers.
55. Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Prog. Retin. Eye. Res. 19, 385-419.