Visual Pigment Evolution in Reptiles

Abstract

The long history and great ecological and morphological diversity of reptiles (all amniotes except mammals and birds) is matched by their visual system diversity. Although less known than in other amniotes, visual pigments have been studied in all extant reptile orders except Sphenodontia. There have been no additions to the five visual pigments present in the ancestral vertebrate, although there have been multiple independent losses. Crocodylians retain three visual pigments, many lizards as well as Testudines four or five and snakes one to three. Adaptive pigment evolution includes tuning site amino acid substitutions and switches between chromophore types that together generate ultraviolet to infrared spectral sensitivity. Reptiles present some of the best evidences of evolutionary rod–cone and cone–rod transmutation with, for example typically cone visual pigments expressed in rod‐like photoreceptors. Reptile visual pigments show evidence of substantial adaptive evolution, at least some of which is associated with major ecological shifts.

Key Concepts

  • Reptiles have no more than five visual pigments, as few as one and typically at least three.
  • Up to four of the ancestral vertebrate visual pigments have been lost independently in different reptile lineages, and no visual opsin gene duplications have been identified so far.
  • Testudines have between four and five visual pigments and a wide range of photoreceptor oil droplets, representing one of the most complex visual pigment systems in tetrapod vertebrates.
  • Despite many of them being nocturnal, no rhodopsin 1 has been detected in geckos.
  • No sws1 or rh2 opsin genes can be detected in genomic sequence data for crocodylians.
  • Among squamates, some lizards have a mixture of A1 and A2 chromophores incorporated in their visual pigments, allowing a wide colour sensitivity, including infrared vision.
  • In the green anole (Anolis carolinensis), only cone opsins have been reported (SWS1, SWS2, RH2 and LWS) in studies of the eye. However, a 515‐nm tuned rh1 rhodopsin gene occurs in the genome of this species.
  • Extant snakes have lost two visual pigments (SWS2 and RH2), likely as an adaptation to a low light environment inhabited by a snake ancestor.
  • Extreme burrowing in scolecophidians (blind, worm and thread snakes) is correlated with the loss of the SWS1 and LWS visual pigments and cones, rendering these snakes rod (RH1) monochromats.
  • The expression of RH1, SWS1 and LWS pigments in snake lineages with seemingly all‐cone and all‐rod retinae suggests multiple transmutations from cone to rod and vice versa in snakes. Similar transmutations likely occurred in some lizards and perhaps crocodylians.
  • Visual pigment spectral sensitivity in reptiles has been found to correlate with the light transmission properties of the ocular media (e.g. snakes) and photoreceptor oil droplets (e.g. testudines), that is the pigments are not sensitive to wavelengths of light filtered out by these structures.

Keywords: cones; photopic vision; rods; scotopic vision; oil droplets; opsins; crocodylians; Testudines; lizards; snakes

Figure 1. Vertebrate visual pigments and corresponding ranges of light sensitivities (λmax).
Figure 2. Two‐dimensional diagram illustrating the seven transmembrane helices (TM) and extra loop (EL) and intracellular loop (CL), showing the arrangement of the helices around the chromophore, shown in orange. Although the helices are of different lengths, for simplicity, each helix is shown with only the central 18 amino acids. The amino acid residues with major impact on the spectral tuning (λmax) are shown, and numbering is based on bovine rod opsin.
Figure 3. Phylogenetic relationships among sauropsids (‘reptiles’ and birds) (based on Modesto and Anderson, and Pyron et al., ), showing visual pigment complements.
Figure 4. Phylogenetic tree of the visual pigments in reptiles and birds.
close

References

Alföldi J, Di Palma F, Grabherr M, et al. (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477: 587–591.

Borges R, Khan I, Johnson WE, et al. (2015) Gene loss, adaptive evolution and the co‐evolution of plumage coloration genes with opsins in birds. BMC Genomics 16: 675.

Bowmaker JK, Loew ER and Ott M (2005) The cone photoreceptors and visual pigments of chameleons. Journal of Comparative Physiology A 191: 925–932.

Bowmaker J and Hunt D (2006) Evolution of vertebrate visual pigments. Current Biology 16: R484–R849.

Buser P and Imbert M (1992) Vision. Cambridge, MA: The MIT Press.

Crescitelli F (1977) The visual pigments of geckos and other vertebrates. In: Crescitelli F (ed) Handbook of Sensory Physiology, pp. 391–450. Berlin: Springer.

Cronin TW, Johnsen S, Marshall NJ and Warrant EJ (2014) Visual pigments and photoreceptors. In: Visual Ecology, pp. 37–65. Princeton, NJ: Princeton University Press.

Davies WL, Cowing JA, Bowmaker JK, et al. (2009) Shedding light on serpent sight: the visual pigments of henophidian snakes. Journal of Neuroscience 29: 7519–7525.

Davies WIL, Collin SP and Hunt DM (2012) Molecular ecology and adaptation of visual photopigments in craniates. Molecular Ecology 21 (13): 3121–3158.

Ellingson JM, Fleishman LJ and Loew ER (1995) Visual pigments and spectral sensitivity of the diurnal gecko Gonatodes albogularis. Journal of Comparative Physiology A 177: 559–567.

Emerling CA and Springer MS (2014) Eyes underground: regression of visual protein networks in subterranean mammals. Molecular Phylogenetics and Evolution 78: 260–270.

Enright JM, Toomey MB, Sato S‐Y, et al. (2015) Cyp27c1 red‐shifts the spectral sensitivity of photoreceptors by converting Vitamin A1 into A2. Current Biology 25 (23): 3048–3057.

Fasick JI and Robinson PR (1998) Mechanism of spectral tuning in the dolphin visual pigments. Biochemistry 37: 433–438.

Fleishman LJ, Loew ER and Whiting MJ (2011) High sensitivity to short wavelengths in a lizard and implications for understanding the evolution of visual systems in lizards. Proceedings of the Royal Society B 278: 2891–2899.

Gerkema MP, Davies WIL, Foster RG, et al. (2013) The nocturnal bottleneck and the evolution of activity patterns in mammals. Proceedings of the Royal Society B 280: 20130508.

Govardovskii VI (1983) On the role of oil drops in colour vision. Vision Research 23: 1739–1740.

Hart NS, Coimbra JP, Collin SP, et al. (2012) Photoreceptor types, visual pigments, and topographic specializations in the retinae of hydrophiid sea snakes. Journal of Comparative Neurology 520: 1246–1261.

Hárosi FI (1994) An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34: 1359–1367.

Hauser FE, van Hazel I and Chang BSW (2014) Spectral tuning in vertebrate short wavelength‐sensitive 1 (SWS1) visual pigments: can wavelength sensitivity be inferred from sequence data?. Journal of Experimental Zoology B: Molecular and Developmental Evolution 322: 529–539.

Horváth G and Varju D (2004) Polarized Light in Animal Vision. Berlin: Springer.

Hsiang AY, Field DJ, Webster TH, et al. (2015) The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology 15: 87.

Hunt DM, Carvalho LS, Cowing JA and Davies WL (2009) Evolution and spectral tuning of visual pigments in birds and mammals. Philosophical Transactions of the Royal Society B: Biological Sciences 364 (1531): 2941–2955. http://doi.org/10.1098/rstb.2009.0044

Kawamura S and Yokoyama S (1997) Expression of visual and nonvisual opsins in American chameleon. Vision Research 37: 1867.

Kochendoerfer G, Lin S, Sakmar T, et al. (1999) How color visual pigments are tuned. Trends in Biochemical Sciences 24: 300–305.

Kos M, Bulog B, Szel A, et al. (2001) Immunocytochemical demonstration of visual pigments in the degenerate retinal and pineal photoreceptors of the blind cave salamander (Proteus anguinus). Cell and Tissue Research 303: 15–25.

Liebman PA and Granda AM (1971) Microspectrophotometric measurements of visual pigments in two species of turtle, Pseudemys scripta and Chelonia mydas. Vision Research 11: 105–114.

Lin SW, Kochendoerfer GG, Carroll KS, et al. (1998) Mechanisms of spectral tuning in blue cone visual pigments: Visible and Raman Spectroscopy of blue‐shifted Rhodopsin mutants. Journal of Biological Chemistry 273: 24583.

Loew ER and Govardovskii VI (2001) Photoreceptors and visual pigments in the red‐eared turtle, Trachemys scripta elegans. Visual Neuroscience 18: 753–757.

Loew ER, Govardovskii VI, Rohlich P, et al. (1996) Microspectrophotometric and immunocytochemical identification of ultraviolet photoreceptors in geckos. Visual Neuroscience 13: 247–256.

Loew ER, Fleishman LJ, Foster RG, et al. (2002) Visual pigments and oil droplets in diurnal lizards: a comparative study of Caribbean anoles. Journal of Experimental Biology 205: 927–938.

Martin M, Le Galliard J‐F, Meylan S, et al. (2015) The importance of ultraviolet and near‐infrared sensitivity for visual discrimination in two species of lacertid lizards. Journal of Experimental Biology 218: 458–465.

Meyer‐Rochow VB, Wohlfahrt S and Ahnelt PK (2005) Photoreceptor cell types in the retina of the tuatara (Sphenodon punctatus) have cone characteristics. Micron 36: 423–428.

Modesto SP and Anderson JS (2004) The phylogenetic definition of reptilia. Systematic Biology 53: 815–821.

Mohun SM, Davies WL, Bowmaker JK, et al. (2010) Identification and characterization of visual pigments in caecilians (Amphibia: Gymnophiona), an order of limbless vertebrates with rudimentary eyes. Journal of Experimental Biology 213: 3586–3592.

Nagloo N, Collin SP, Hemmi JM and Hart NS (2016) Spatial resolving power and spectral sensitivity of the saltwater crocodile, Crocodylus porosus, and the freshwater crocodile, Crocodylus johnstoni. Journal of Experimental Biology 219: 1394–1404. The Company of Biologists Ltd.

Ohtsuka T (1985a) Relation of spectral types to oil droplets in cones of turtle retina. Science 229: 874–877.

Ohtsuka T (1985b) Spectral sensitivities of seven morphological types of photoreceptors in the retina of the turtle, Geoclemys reevesii. Journal of Comparative Neurology 237: 145–154.

Pyron R, Burbrink FT and Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13: 93.

Schott RK, Müller J, Yang CGY, et al. (2016) Evolutionary transformation of rod photoreceptors in the all‐cone retina of a diurnal garter snake. Proceedings of the National Academy of Sciences of the United States of America 113 (2): 356–361.

Shedlock AM and Edwards SV (2009) Amniotes (Amniota). In: Blair Hedges S and Kumar S (eds) The Timetree of Life, pp. 375–379. New York: Oxford University Press.

Sillman AJ, Ronan SJ and Loew ER (1991) Histology and microspectrophotometry of the photoreceptors of a crocodilian, Alligator mississippiensis. Proceedings of the Royal Society B 243: 93–98.

Sillman AJ, Govardovskii VI, Rohlich P, et al. (1997) The photoreceptors and visual pigments of the garter snake (Thamnophis sirtalis): a microspectrophotometric, scanning electron microscopic and immunocytochemical study. Journal of Comparative Physiology A 181: 89.

Sillman AJ, Carver JK and Loew ER (1999) The photoreceptors and visual pigments in the retina of a boid snake, the ball python (Python regius). Journal of Experimental Biology 202: 1931–1938.

Sillman AJ, Johnson JL and Loew ER (2001) Retinal photoreceptors and visual pigments in Boa constrictor imperator. Journal of Experimental Zoology 290: 359–365.

Simões BF, Sampaio FL, Jared C, et al. (2015) Visual system evolution and the nature of the ancestral snake. Journal of Evolutionary Biology 28: 1309–1320.

Simões BF, Sampaio FL, Loew ER, et al. (2016a) Multiple rod‐cone and cone‐rod photoreceptor transmutations in snakes: evidence from visual opsin gene expression. Proceedings of the Royal Society B 283 (1823pii: 20152624).

Simões BF, Sampaio FL, Douglas RH, et al. (2016b) Visual pigments, ocular filters and the evolution of snake vision. Molecular Biology and Evolution 33: 2483–2495.

Su C‐Y, Luo D‐G, Terakita A, et al. (2006) Parietal‐eye phototransduction components and their potential evolutionary implications. Science 311: 1617–1621.

Underwood G (1970) The eye. In: Gans C and Parsons TS (eds) Biology of the Reptilia: Morphology B, vol. 2, pp. 1–97. New York: Academic Press.

Walls GL (1942) The Vertebrate Eye and Its Adaptive Radiation. New York: Fafner Publishing Company.

Yokoyama S (2008) Evolution of dim‐light and color vision pigments. Annual Review of Genomics and Human Genetics 9: 259–282.

Yokoyama S, Xing J, Liu Y, et al. (2014) Epistatic adaptive evolution of human color vision. PLoS Genetics 10: e1004884.

Further Reading

Reuter T and Peichl L (2008) Structure and Function of the Retina in Aquatic Tetrapods. In: Thewissen JGM and Sirpa Nummela (eds) Sensory Evolution on the Threshold: Adaption in Secondarily Aquatic Vertebrates, pp. 149–172. Berkeley, CA: University of California Press.

Schwab IR (2012) Evolution's Witness: How Eyes Evolved. Oxford: Oxford University Press.

Vitt LJ and Caldwell JP (2014) Herpetology. An Introductory Biology of Amphibians and Reptiles, 4th edn. San Diego, CA: Academic Press.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Simões, Bruno F, and Gower, David J(Jun 2017) Visual Pigment Evolution in Reptiles. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0026519]