Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-18T03:47:04.822Z Has data issue: false hasContentIssue false
  • English
  • Français

The retinal pigments of the whale shark (Rhincodon typus) and their role in visual foraging ecology

Published online by Cambridge University Press:  13 November 2019

Jeffry I. Fasick ,
Haya Algrain ,
Katherine M. Serba  and
Phyllis R. Robinson
Jeffry I. Fasick*
Affiliation:
Department of Biological Sciences, The University of Tampa, Tampa, Florida 33606
Haya Algrain
Affiliation:
Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland 21250
Katherine M. Serba
Affiliation:
Department of Biological Sciences, The University of Tampa, Tampa, Florida 33606
Phyllis R. Robinson
Affiliation:
Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland 21250
*
*Address correspondence to: Jeffry I. Fasick, Email: jfasick@ut.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The spectral tuning properties of the whale shark (Rhincodon typus) rod (rhodopsin or Rh1) and long-wavelength-sensitive (LWS) cone visual pigments were examined to determine whether these retinal pigments have adapted to the broadband light spectrum available for surface foraging or to the narrowband blue-shifted light spectrum available at depth. Recently published whale shark genomes have identified orthologous genes for both the whale shark Rh1 and LWS cone opsins suggesting a duplex retina. Here, the whale shark Rh1 and LWS cone opsin sequences were examined to identify amino acid residues critical for spectral tuning. Surprisingly, the predicted absorbance maximum (λmax) for both the whale shark Rh1 and LWS visual pigments is near 500 nm. Although Rh1 λmax values near 500 nm are typical of terrestrial vertebrates, as well as surface foraging fish, it is uncommon for a vertebrate LWS cone pigment to be so greatly blue-shifted. We propose that the spectral tuning properties of both the whale shark Rh1 and LWS cone pigments are most likely adaptations to the broadband light spectrum available at the surface. Whale shark melanopsin (Opn4) deactivation kinetics was examined to better understand the underlying molecular mechanisms of the pupillary light reflex. Results show that the deactivation rate of whale shark Opn4 is similar to the Opn4 deactivation rate from vertebrates possessing duplex retinae and is significantly faster than the Opn4 deactivation rate from an aquatic rod monochromat lacking functional cone photoreceptors. The rapid deactivation rate of whale shark Opn4 is consistent with a functional cone class and would provide the animal with an exponential increase in the number of photons required for photoreceptor signaling when transitioning from photopic to scotopic light conditions, as is the case when diving.

Keywords

Whale sharkVisual pigmentsMelanopsinForaging ecology
Type
Research Article
Information
Visual Neuroscience , Volume 36 , 2019 , E011
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asenjo, A.B., Rim, J. & Oprian, D.D. (1994). Molecular determinants of human red/green color discrimination. Neuron 12, 1131–1138.CrossRefGoogle ScholarPubMed
Bailes, H.J. & Lucas, R.J. (2013). Human melanopsin forms a pigment maximally sensitive to blue light (λ max ≈ 479 nm) supporting activation of Gq/11 and Gi/o signaling cascades. Proceedings of the Royal Society B: 280, 20122987.CrossRefGoogle Scholar
Blasic, J.R., Brown, R.L. & Robinson, P.R. (2012). Light-dependent phosphorylation of the carboxy tail of mouse melanopsin. Cellular and Molecular Life Sciences 69, 1551–1562.CrossRefGoogle ScholarPubMed
Blasic, J.R., Matos-Cruz, V., Ujla, D., Cameron, E.G., Hattar, S., Halpern, M.E. & Robinson, P.R. (2014). Identification of critical phosphorylation sites on the carboxy tail of melanopsin. Biochemistry 53, 2644–2649.CrossRefGoogle ScholarPubMed
Bowmaker, J., Govardovskii, V., Shukolyukov, S., Zueva, J.L., Hunt, D., Sideleva, V. & Smirnova, O. (1994). Visual pigments and the photic environment: The cottoid fish of lake baikal. Vision Research 34, 591–605.CrossRefGoogle ScholarPubMed
Brunnschweiler, J., Baensch, H., Pierce, S. & Sims, D. (2009). Deep-diving behaviour of a whale shark Rhincodon typus during long-distance movement in the western Indian Ocean. Journal of Fish Biology 74, 706–714.CrossRefGoogle ScholarPubMed
Clark, E. & Nelson, D.R. (1997). Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico. Environmental Biology of Fishes 50, 63–73.CrossRefGoogle Scholar
Collette, F., Renger, T., Müh, F. & am Busch, Marcel Schmidt (2018). Red/green color tuning of visual rhodopsins: Electrostatic theory provides a quantitative explanation. The Journal of Physical Chemistry B 122, 4828–4837.CrossRefGoogle ScholarPubMed
Compagno, L.J.V. (1984). FAO species catalogue. Vol. 4. Sharks of the world: An annotated and illustrated catalogue of shark species known to date. Part 2. Carcharhiniformes. FAO Fish. Synop. 125, 251–655.Google Scholar
Croll, D.A., Acevedo-Gutierrez, A., Tershy, B.R. & Urban-Ramirez, J.J.C.B. (2001). The diving behavior of blue and fin whales: Is dive duration shorter than expected based on oxygen stores? Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 129, 797–809.CrossRefGoogle ScholarPubMed
Cronin, T.W., Johnsen, S., Marshall, N.J. & Warrant, E.J. (2014). Visual Ecology. Princeton: Princeton University Press.CrossRefGoogle Scholar
Davies, W.L., Carvalho, L.S., Tay, B.H., Brenner, S., Hunt, D.M. & Venkatesh, B. (2009). Into the blue: Gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Research 19, 415–426.CrossRefGoogle Scholar
Davies, W.I.L., Tay, B.H., Zheng, L., Danks, J.A., Brenner, S., Foster, R.G., Collin, S.P., Hankins, M.W., Venkatesh, B. & Hunt, D.M. (2012). Evolution and functional characterization of melanopsins in a deep-sea chimaera (elephant shark, Callorhinchus milii). PLoS One 7, e51276.CrossRefGoogle Scholar
Denton, E. & Shaw, T. (1963). The visual pigments of some deep-sea elasmobranchs. Journal of the Marine Biological Association of the United Kingdom 43, 65–70.CrossRefGoogle Scholar
Denton, E. & Warren, F. (1956). Visual pigments of deep-sea fish. Nature 178, 1059.CrossRefGoogle ScholarPubMed
Denton, E. & Warren, F. (1957). The photosensitive pigments in the retinae of deep-sea fish. Journal of the Marine Biological Association of the United Kingdom 36, 651–662.CrossRefGoogle Scholar
Douglas, R., Partridge, J. & Marshall, N.J. (1998). The eyes of deep-sea fish I: Lens pigmentation, tapeta and visual pigments. Progress in Retinal and Eye Research 17, 597–636.CrossRefGoogle Scholar
Douglas, R. & Partridge, J. (1997). On the visual pigments of deep-sea fish. Journal of Fish Biology 50, 68–85.CrossRefGoogle Scholar
Ernst, O.P., Lodowski, D.T., Elstner, M., Hegemann, P., Brown, L.S. & Kandori, H. (2013). Microbial and animal rhodopsins: Structures, functions, and molecular mechanisms. Chemical Reviews 114, 126–163.CrossRefGoogle ScholarPubMed
Fasick, J.I. & Robinson, P.R. (1998). Mechanism of spectral tuning in the dolphin visual pigments. Biochemistry 37, 433–438.CrossRefGoogle ScholarPubMed
Franke, R., Sakmar, T., Oprian, D. & Khorana, H. (1988). A single amino acid substitution in rhodopsin (lysine 248----leucine) prevents activation of transducin. Journal of Biological Chemistry 263, 2119–2122.Google ScholarPubMed
Goldbogen, J.A., Calambokidis, J., Friedlaender, A.S., Francis, J., Deruiter, S.L., Stimpert, A.K., Falcone, E. & Southall, B.L. (2013). Underwater acrobatics by the world’s largest predator: 360 rolling manoeuvres by lunge-feeding blue whales. Biology Letters 9, 20120986.CrossRefGoogle ScholarPubMed
Goldbogen, J.A., Calambokidis, J., Shadwich, R.E., Oleson, E.M., Mcdonald, M.A. & Hildebrand, J.A. (2006). Kinematics of foraging dives and lunge-feeding in fin whales. Journal of Experimental Biology 209, 1231–1244.CrossRefGoogle ScholarPubMed
Hao, W. & Fong, H.K. (1996). Blue and ultraviolet light-absorbing opsin from the retinal pigment epithelium. Biochemistry 35, 6251–6256.CrossRefGoogle ScholarPubMed
Hara, Y., Yamaguchi, K., Onimaru, K., Kadota, M., Koyanagi, M., Keeley, S.D., Tatsumi, K., Tanaka, K., Motone, F. & Kageyama, Y. (2018). Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates. Nature Ecology & Evolution 2, 1761.CrossRefGoogle ScholarPubMed
Hart, N.S., Theiss, S.M., Harahush, B.K. & Collin, S.P. (2011). Microspectrophotometric evidence for cone monochromacy in sharks. Naturwissenschaften 98, 193–201.CrossRefGoogle ScholarPubMed
Heide, K.L.L.M.P. & Nielsen, T.G. (2007). Role of the bowhead whale as a predator in West Greenland. Marine Ecology Progress Series 346, 285–297.Google Scholar
Heyman, W.D., Graham, R.T., Kjerfve, B. & Johannes, R.E. (2001). Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Marine Ecology Progress Series 215, 275–282.CrossRefGoogle Scholar
Hunt, D.M., Dulai, K.S., Partridge, J.C., Cottrill, P. & Bowmaker, J.K. (2001). The molecular basis for spectral tuning of rod visual pigments in deep-sea fish. Journal of Experimental Biology 204, 3333–3344.Google ScholarPubMed
Johnsen, S., Kelber, A., Warrant, E., Sweeney, A.M., Widder, E.A., Lee, R.L. & Hernandez-Andres, J. (2006). Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. Journal of Experimental Biology 209, 789–800.CrossRefGoogle ScholarPubMed
Johnsen, S. (2012). The Optics of Life: A Biologist’s Guide to Light in Nature. Princeton: Princeton University Press.CrossRefGoogle Scholar
Keane, M., Semeiks, J., Webb, A.E., Li, Y.I., Quesada, V., Craig, T., Madsen, L.B., Van Dam, S., BraWand, D. & Marques, P.I. (2015). Insights into the evolution of longevity from the bowhead whale genome. Cell Reports 10, 112–122.CrossRefGoogle ScholarPubMed
Koyanagi, M., Kubokawa, K., Tsukamoto, H., Shichida, Y. & Terakita, A. (2005). Cephalochordate melanopsin: Evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Current Biology 15, 1065–1069.CrossRefGoogle ScholarPubMed
Koyanagi, M., Terakita, A., Kubokawa, K. & Shichida, Y. (2002). Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis-and all-trans-retinals as their chromophores. FEBS Letters 531, 525–528.CrossRefGoogle ScholarPubMed
Lin, S.W., Kochendoerfer, G.G., Carroll, K.S., Wang, D., Mathies, R.A. & Sakmar, T.P. (1998). Mechanisms of spectral tuning in blue cone visual pigments visible and Raman spectroscopy of blue-shifted rhodopsin mutants. Journal of Biological Chemistry 273, 24583–24591.CrossRefGoogle ScholarPubMed
Loew, E. & Lythgoe, J. (1978). The ecology of cone pigments in teleost fishes. Vision Research 18, 715–722.CrossRefGoogle ScholarPubMed
Losey, G., Mcfarland, W., Loew, E., Zamzow, J., Nelson, P. & Marshall, N.J. (2003). Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003, 433–454.CrossRefGoogle Scholar
Lythgoe, J., Muntz, W., Partridge, J., Shand, J. & Williams, D.M. (1994). The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. Journal of Comparative Physiology 174, 461–467.Google Scholar
Maisey, J. (1984). Higher elasmobranch phylogeny and biostratigraphy. Zoological Journal of the Linnean Society 82, 33–54.CrossRefGoogle Scholar
Meekan, M., Fuiman, L., Davis, R., Berger, Y. & Thums, M. (2015). Swimming strategy and body plan of the world’s largest fish: Implications for foraging efficiency and thermoregulation. Frontiers in Marine Science 2, 64.CrossRefGoogle Scholar
Meredith, R.W., Gatesy, J., Emerling, C.A., York, V.M. & Springer, M.S. (2013). Rod monochromacy and the coevolution of cetacean retinal opsins. PLoS Genetics 9, e1003432.CrossRefGoogle ScholarPubMed
Motta, P.J., Maslanka, M., Hueter, R.E., Davis, R.L., De La Parra, R., Mulvany, S.L., Habegger, M.L., Strother, J.A., Mara, K.R. & Gardiner, J.M. (2010). Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113, 199–212.CrossRefGoogle ScholarPubMed
Munz, F.W. (1957). Photosensitive pigments from retinas of deep-sea fishes. Science 125, 1142–1143.CrossRefGoogle ScholarPubMed
Murakami, M. & Kouyama, T. (2008). Crystal structure of squid rhodopsin. Nature 453, 363–367.CrossRefGoogle ScholarPubMed
Musilova, Z., Cortesi, F., Matschiner, M., Davies, W.I., Patel, J.S., Stieb, S.M., De Busserolles, F., Malmstrøm, M., Tørresen, O.K., Brown, C.J., Mountford, J.K., Hanel, R. Stenkamp, D.L., Jakobsen, K.S., Carleton, K.L., Jentoft, S., Marshall, J. & Salzburger, W. (2019). Vision using multiple distinct rod opsins in deep-sea fishes. Science 364, 588–592.CrossRefGoogle ScholarPubMed
Naylor, G.J., Caira, J.N., Jensen, K., Rosana, K.A., Straube, N. & Lakner, C. (2012). Elasmobranch phylogeny: A mitochondrial estimate based on 595 species. In Biology of Sharks and Their Relatives, ed. Carrier, J.C., Musick, J.A., & Heithaus, M.R., pp. 31–56. Boca Raton, FL USA: CRC Press.CrossRefGoogle Scholar
Nelson, J.D. & Eckert, S.A. (2007). Foraging ecology of whale sharks (Rhincodon typus) within bahía de Los angeles, baja California norte, méxico. Fisheries Research 84, 47–64.CrossRefGoogle Scholar
Okada, T., Sugihara, M., Bondar, A.N., Elstner, M., Entel, P. & Buss, V. (2004). The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure. Journal of Molecular Biology 342, 571–583.CrossRefGoogle ScholarPubMed
Oprian, D.D., Molday, R.S., Kaufman, R.J. & Khorana, H.G. (1987). Expression of a synthetic bovine rhodopsin gene in monkey kidney cells. Proceedings of the National Academy of Sciences 84, 8874–8878.CrossRefGoogle ScholarPubMed
Palczewski, K., Kumasaka, T., Hori, T., Behnke, C.A., Motoshima, H., Fox, B.A., Le Trong, I., Teller, D.C., Okada, T. & Stenkamp, R.E. (2000). Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739–745.CrossRefGoogle ScholarPubMed
Panda, S., Nayak, S.K., Campo, B., Walker, J.R., Hogenesch, J.B. & Jegla, T. (2005). Illumination of the melanopsin signaling pathway. Science 307, 600–604.CrossRefGoogle ScholarPubMed
Panigada, S., Zanardelli, M., Canese, S. & Jahoda, M. (1999). How deep can baleen whales dive? Marine Ecology Progress Series 187, 309–311.CrossRefGoogle Scholar
Parks, S.E., Warren, J.D., Stamieszkin, K., Mayo, C.A. & Wiley, D. (2011). Dangerous dining: Surface foraging of north atlantic right whales increases risk of vessel collisions. Biology Letters 8, 57–60.CrossRefGoogle ScholarPubMed
Provencio, I., Rodriguez, I.R., Jiang, G., Hayes, W.P., Moreira, E.F. & Rollag, M.D. (2000). A novel human opsin in the inner retina. Journal of Neuroscience 20, 600–605.CrossRefGoogle ScholarPubMed
Qiu, X., Kumbalasiri, T., Carlson, S.M., Wong, K.Y., Krishna, V., Provencio, I. & Berson, D.M. (2005). Induction of photosensitivity by heterologous expression of melanopsin. Nature 433, 745–749.CrossRefGoogle ScholarPubMed
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014). FigTree v1.4.4. Available at: http://tree.bio.ed.ac.uk/software/figtree.Google Scholar
Read, T.D., Petit, R.A., Joseph, S.J., Alam, M.T., Weil, M.R., Ahmad, M., Bhimani, R., Vuong, J.S., Haase, C.P. & Webb, D.H. (2017). Draft sequencing and assembly of the genome of the world’s largest fish, the whale shark: Rhincodon typus Smith 1828. BMC Genomics 18, 532.CrossRefGoogle ScholarPubMed
Schweikert, L.E., Fasick, J.I. & Grace, M.S. (2016). Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina. Journal of Comparative Neurology 524, 2873–2885.CrossRefGoogle ScholarPubMed
Schweikert, L.E., Caves, E.M., Solie, S.E., Sutton, T.T. & Johnsen, S. (2018). Variation in rod spectral sensitivity of fishes is best predicted by habitat and depth. Journal of Fish Biology 95, 179–185.CrossRefGoogle Scholar
Sekharan, S., Katayama, K., Kandori, H. & Morokuma, K. (2012). Color vision: “OH-site” rule for seeing red and green. Journal of the American Chemical Society 134, 10706–10712.CrossRefGoogle ScholarPubMed
Shanmugam, P. & Ahn, Y. (2007). Reference solar irradiance spectra and consequences of their disparities in remote sensing of the ocean colour. Annales Geophysicae 25, 1235–1252.CrossRefGoogle Scholar
Somasundaram, P., Wyrick, G.R., Fernandez, D.C., Ghahari, A., Pinhal, C.M., Richardson, M.S., Rupp, A.C., Cui, L., Wu, Z. & Brown, R.L. (2017). C-terminal phosphorylation regulates the kinetics of a subset of melanopsin-mediated behaviors in mice. Proceedings of the National Academy of Sciences 114, 2741–2746.CrossRefGoogle ScholarPubMed
Sun, H., Macke, J.P. & Nathans, J. (1997). Mechanisms of spectral tuning in the mouse green cone pigment. Proceedings of the National Academy of Sciences 94, 8860–8865.CrossRefGoogle ScholarPubMed
Sweeney, A.M., Boch, C.A., Johnsen, S. & Morse, D.E. (2011). Twilight spectral dynamics and the coral reef invertebrate spawning response. Journal of Experimental Biology 214, 770–777.CrossRefGoogle ScholarPubMed
Taylor, J.G. (2007). Ram filter-feeding and nocturnal feeding of whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Fisheries Research 84, 65–70.CrossRefGoogle Scholar
Taylor, S.M., Loew, E.R. & Grace, M.S. (2011). Developmental shifts in functional morphology of the retina in Atlantic tarpon, Megalops atlanticus (Elopomorpha: Teleostei) between four ecologically distinct life-history stages. Visual Neuroscience 28, 309–323.CrossRefGoogle ScholarPubMed
Torii, M., Ojima, D., Okano, T., Nakamura, A., Terakita, A., Shichida, Y., Wada, A. & Fukada, Y. (2007). Two isoforms of chicken melanopsins show blue light sensitivity. FEBS Letters 581, 5327–5331.CrossRefGoogle ScholarPubMed
Vélez-zuazo, X. & Agnarsson, I. (2011). Shark tales: A molecular species-level phylogeny of sharks (Selachimorpha, chondrichthyes). Molecular Phylogenetics and Evolution 58, 207–217.CrossRefGoogle Scholar
Wiley, D., Ware, C., Bocconcelli, A., Cholewiak, D., Friedlaender, A., Thompson, M. & Weinrich, M. (2011). Underwater components of humpback whale bubble-net feeding behaviour. Behaviour 148, 575–602.Google Scholar
Wu, S. & Zhang, Y. (2007). Lomets: A local meta-threading-server for protein structure prediction. Nucleic Acids Research 35, 3375–3382.CrossRefGoogle ScholarPubMed
Yokoyama, S. (2008). Evolution of dim-light and color vision pigments. Annual Review of Genomics and Human Genetics 9, 259–282.CrossRefGoogle ScholarPubMed
Yokoyama, S., Tada, T., Zhang, H. & Britt, L. (2008). Elucidation of phenotypic adaptations: Molecular analyses of dim-light vision proteins in vertebrates. Proceedings of the National Academy of Sciences 105, 13480–13485.CrossRefGoogle ScholarPubMed