Skip to main content
Log in

The Coevolution of Blue-Light Photoreception and Circadian Rhythms

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Sunlight is a primary source of energy for life. However, its UV component causes DNA damage. We suggest that the strong UV component of sunlight contributed to the selective pressure for the evolution of the specialized photoreceptor cryptochrome from photolyases involved in DNA repair and propose that early metazoans avoided irradiation by descending in the oceans during the daytime. We suggest further that it is not coincidental that blue-light photoreception evolved in an aquatic environment, since only blue light can penetrate to substantial depths in water. These photoreceptors were then also critical for sensing the decreased luminescence that signals the coming of night and the time to return to the surface. The oceans and the 24-h light–dark cycle therefore provided an optimal setting for an early evolutionary relationship between blue-light photoreception and circadian rhythmicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. DM Berson FA Dunn M Takao (2002) ArticleTitlePhototransduction by retinal ganglion cells that set the circadian clock. Science 295 1070–1073 Occurrence Handle1:CAS:528:DC%2BD38Xht1Gru7g%3D Occurrence Handle11834835

    CAS  PubMed  Google Scholar 

  2. BP Boden EM Kampa (1967) ArticleTitleThe influence of natural light on the vertical migrations of an animal community in the sea. Symp Zool Soc Lond 19 15–26

    Google Scholar 

  3. BG Bogorov (1946) ArticleTitlePeculiarities of diurnal vertical migrations of zooplankton in polar seas. J Mar Res 6 25–36

    Google Scholar 

  4. AR Cashmore JA Jarillo YJ Wu D Liu (1999) ArticleTitleCryptochromes: blue light receptors for plants and animals. Science 284 760–765 Occurrence Handle10.1126/science.284.5415.760 Occurrence Handle1:CAS:528:DyaK1MXivVKksL4%3D Occurrence Handle10221900

    Article  CAS  PubMed  Google Scholar 

  5. DH Cushing (1951) ArticleTitleThe vertical migration of planktonic Crustacea. Biol Rev Cambr Philos Soc 26 158–192

    Google Scholar 

  6. G Cuvier (1829) Le règne animal. Déterville Paris 164–171

    Google Scholar 

  7. PF Devlin SA Kay (2000) ArticleTitleCryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell 12 2499–2510 Occurrence Handle1:CAS:528:DC%2BD3MXns1Sgtw%3D%3D Occurrence Handle11148293

    CAS  PubMed  Google Scholar 

  8. ES Egan TM Franklin MJ Hilderbrand-Chae GP McNeil MA Roberts AJ Schroeder X Zhang FR Jackson (1999) ArticleTitleAn extraretinally expressed insect cryptochrome with similarity to the blue light photoreceptors of mammals and plants. J Neurosci 19 3665–3673 Occurrence Handle1:CAS:528:DyaK1MXjtV2ktrk%3D Occurrence Handle10233998

    CAS  PubMed  Google Scholar 

  9. P Emery WV So M Kaneko JC Hall M Rosbash (1998) ArticleTitleCRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95 669–679 Occurrence Handle1:CAS:528:DyaK1cXnvFynurw%3D Occurrence Handle9845369

    CAS  PubMed  Google Scholar 

  10. P Emery R Stanewsky JC Hall M Rosbash (2000) ArticleTitleA unique circadian-rhythm photoreceptor. Nature 404 456–457 Occurrence Handle1:CAS:528:DC%2BD3cXisVyjtrg%3D Occurrence Handle10761904

    CAS  PubMed  Google Scholar 

  11. EM Fleischmann (1989) ArticleTitleThe measurement and penetration of ultraviolet radiation into tropical marine water. Limnol Oceanogr 34 1623–1629

    Google Scholar 

  12. JJ Gooley J Lu TC Chou TE Scammell CB Saper (2001) ArticleTitleMelanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4 1165 Occurrence Handle1:CAS:528:DC%2BD3MXovVCqur4%3D Occurrence Handle11713469

    CAS  PubMed  Google Scholar 

  13. J Hannibal P Hindersson SM Knudsen B Georg J Fahrenkrug (2002) ArticleTitleThe photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22 RC191 Occurrence Handle11756521

    PubMed  Google Scholar 

  14. S Hattar HW Liao M Takao DM Berson KW Yau (2002) ArticleTitleMelanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science 295 1065–1070 Occurrence Handle1:CAS:528:DC%2BD38Xht1Gru7o%3D Occurrence Handle11834834

    CAS  PubMed  Google Scholar 

  15. C Helfrich-Forster C Winter A Hofbauer JC Hall R Stanewsky (2001) ArticleTitleThe circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30 249–261 Occurrence Handle11343659

    PubMed  Google Scholar 

  16. AG Huntsman (1924) ArticleTitleLimiting factors for marine animals. The lethal effect of sunlight. Contrib Can Biol 2 82–88

    Google Scholar 

  17. AB Klugh (1930) ArticleTitleThe effect of the ultraviolet component of the sun’s radiation upon aquatic organisms. Can J Res 2 312–317

    Google Scholar 

  18. B Krishnan JD Levine MK Lynch HB Dowse P Funes JC Hall PE Hardin SE Dryer (2001) ArticleTitleA new role for cryptochrome in a Drosophila circadian oscillator. Nature 411 313–317 Occurrence Handle1:CAS:528:DC%2BD3MXjvF2qtbw%3D Occurrence Handle11357134

    CAS  PubMed  Google Scholar 

  19. K Kume MJ Zylka S Sriram LP Shearman DR Weaver X Jin ES Maywood MH Hastings SM Reppert (1999) ArticleTitlemCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98 193–205 Occurrence Handle1:CAS:528:DyaK1MXltVOqt7c%3D Occurrence Handle10428031

    CAS  PubMed  Google Scholar 

  20. W Lampert (1993) ArticleTitleUltimate causes of diel vertical migration of zooplankton: New evidence for the predator-avoidance hypothesis. Arch Hydrobiol 39 79–88

    Google Scholar 

  21. DM Leech CE Williamson (2001) ArticleTitleIn situ exposure to ultraviolet radiation alters depth distribution of Daphnia. Limnol Oceanogr 46 416–420

    Google Scholar 

  22. JM Lin VL Kilman K Keegan B Paddock M Emery-Le M Rosbash R Allada (2002) ArticleTitleA role for casein kinase 2alpha in the Drosophila circadian clock. Nature 420 816–820 Occurrence Handle10.1038/nature01235 Occurrence Handle1:CAS:528:DC%2BD38XpsFygt7k%3D Occurrence Handle12447397

    Article  CAS  PubMed  Google Scholar 

  23. JW Nybakken (2001) Marine biology: An ecological approach, 5th ed. Benjamin Cummings San Francisco

    Google Scholar 

  24. MD Ohman (1990) ArticleTitleThe demographic benefits of diel vertical migration by zooplankton. Ecol Monogr 60 257–281

    Google Scholar 

  25. S Okano S Kanno M Takao AP Eker K Isono Y Tsukahara A Yasui (1999) ArticleTitleA putative blue-light receptor from Drosophila melanogaster. Photochem Photobiol 69 108–113 Occurrence Handle10.1562/0031-8655(1999)069<0108:APBLRF>2.3.CO;2 Occurrence Handle1:CAS:528:DyaK1MXmtlGqsQ%3D%3D Occurrence Handle10063806

    Article  CAS  PubMed  Google Scholar 

  26. JT Pennington RB Emlet (1986) ArticleTitleOntogenetic and diel vertical migration of a planktonic echinoid larva, Dendraster excentricus (Escholtz): Occurrence, causes and probable consequences. Exp Mar Biol Ecol 104 69–95 Occurrence Handle10.1016/0022-0981(86)90098-5

    Article  Google Scholar 

  27. CS Pittendrigh (1993) ArticleTitleTemporal organization: Reflections of a Darwinian clock-watcher. Annu Rev Physiol 55 17–54 Occurrence Handle10.1146/annurev.ph.55.030193.000313

    Article  Google Scholar 

  28. I Provencio IR Rodriguez G Jiang WP Hayes EF Moreira MD Rollag (2000) ArticleTitleA novel human opsin in the inner retina. J Neurosci 20 600–605 Occurrence Handle1:CAS:528:DC%2BD3cXhtF2hsb8%3D Occurrence Handle10632589

    CAS  PubMed  Google Scholar 

  29. I Provencio MD Rollag AM Castrucci (2002) ArticleTitlePhotoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415 493 Occurrence Handle1:CAS:528:DC%2BD38Xht1Gis74%3D

    CAS  Google Scholar 

  30. A Sancar (1994) ArticleTitleStructure and function of DNA photolyase. Biochemistry 33 2–9 Occurrence Handle1:CAS:528:DyaK2cXkvV2ntw%3D%3D Occurrence Handle8286340

    CAS  PubMed  Google Scholar 

  31. A Sancar (2000) ArticleTitleCryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annu Rev Biochem 69 31–67 Occurrence Handle1:CAS:528:DC%2BD3cXnt1ajtLw%3D Occurrence Handle10966452

    CAS  PubMed  Google Scholar 

  32. JW Schopf JM Hayes MR Walter (1983) Earth’s Earliest Biosphere: Evolution of the earth’s earliest ecosystems: Recent progress and unsolved problems. Princeton University Press Princeton, NJ 361–384

    Google Scholar 

  33. CP Selby A Sancar (1999) ArticleTitleA third member of the photolyase/blue-light photoreceptor family in Drosophila: a putative circadian photoreceptor. Photochem Photobiol 69 105–107 Occurrence Handle10.1562/0031-8655(1999)069<0105:ATMOTP>2.3.CO;2 Occurrence Handle1:CAS:528:DyaK1MXmtlGqsA%3D%3D Occurrence Handle10063805

    Article  CAS  PubMed  Google Scholar 

  34. CP Selby C Thompson TM Schmitz RN Van Gelder A Sancar (2000) ArticleTitleFunctional redundancy of cryptochromes and classical photoreceptors for nonvisual ocular photoreception in mice. Proc Natl Acad Sci USA 97 14697–14702 Occurrence Handle10.1073/pnas.260498597 Occurrence Handle1:CAS:528:DC%2BD3MXitVGgsg%3D%3D Occurrence Handle11114194

    Article  CAS  PubMed  Google Scholar 

  35. KC Smith ER Macagno (1990) ArticleTitleUV photoreceptors in the compound eye of Daphnia magna (Crustacea, Branchiopoda). A fourth spectral class in single ommatidia. J Comp Physiol A 166 597–606 Occurrence Handle1:STN:280:By%2BB2Mjos1Y%3D Occurrence Handle2341987

    CAS  PubMed  Google Scholar 

  36. R Stanewsky M Kaneko P Emery B Beretta K Wager-Smith SA Kay M Rosbash JC Hall (1998) ArticleTitleThe cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95 681–692 Occurrence Handle1:CAS:528:DyaK1cXnvFynuro%3D Occurrence Handle9845370

    CAS  PubMed  Google Scholar 

  37. UC Storz RJ Paul (1998) ArticleTitlePhototaxis in water fleas (Daphnia magna) is differently influenced by visible and UV light. J Comp Physiol A 183 709–717

    Google Scholar 

  38. CL Thompson WS Blaner RN Van Gelder K Lai L Quadro V Colantuoni ME Gottesman A Sancar (2001) ArticleTitlePreservation of light signaling to the suprachiasmatic nucleus in vitamin A-deficient mice. Proc Natl Acad Sci USA 98 11708–11713 Occurrence Handle10.1073/pnas.201301498 Occurrence Handle1:CAS:528:DC%2BD3MXnt12jsbo%3D Occurrence Handle11562477

    Article  CAS  PubMed  Google Scholar 

  39. T Todo H Ryo K Yamamoto H Toh T Inui H Ayaki T Nomura M Ikenaga (1996) ArticleTitleSimilarity among the Drosophila (6-4) photolyase, a human photolyase homolog, and the DNA photolyase-blue-light photoreceptor family. Science 272 109–112 Occurrence Handle1:CAS:528:DyaK28XitVKktLg%3D Occurrence Handle8600518

    CAS  PubMed  Google Scholar 

  40. GT van der Horst M Muijtjens K Kobayashi R Takano S Kanno M Takao J de Wit A Verkerk AP Eker D van Leenen R Buijs D Bootsma JH Hoeijmakers A Yasui (1999) ArticleTitleMammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398 627–630 Occurrence Handle10217146

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Walter Gehring.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gehring, W., Rosbash, M. The Coevolution of Blue-Light Photoreception and Circadian Rhythms . J Mol Evol 57 (Suppl 1), S286–S289 (2003). https://doi.org/10.1007/s00239-003-0038-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-0038-8

Keywords

Navigation