Resumen
Los ritmos biológicos son una parte fundamental de la vida de los organismos y están estrechamente relacionados con movimientos geológicos y cambios ambientales periódicos, como temperatura, humedad y luz. Estos ritmos biológicos se han desarrollado a lo largo del tiempo como una respuesta evolutiva a las presiones ambientales, lo que ha llevado a la formación de circuitos genéticos que controlan el tiempo biológico y regulan la fisiología y el comportamiento de los seres vivos. La percepción de la luz es un factor clave en el desarrollo de los ritmos biológicos, ya que proporciona una señal externa para ajustar los relojes biológicos internos de los organismos. Las fotoliasas y los mecanismos de fotopercepción desarrollados en los seres vivos a lo largo de la evolución han permitido la adaptación a estas señales y la formación del sistema circadiano, responsable de regular los ritmos biológicos diarios y anuales. En todos los seres vivos existe un sistema circadiano; en los mamíferos, este se encuentra en el núcleo supraquiasmático. El circuito genético del reloj interno de los organismos está bien establecido en todos los niveles del organismo, y es esencial para regular comportamientos fundamentales como la alimentación, la reproducción o los procesos migratorios. Los ritmos biológicos también desempeñan un papel importante en la adaptación de organismos a diferentes zonas geográficas y cambios estacionales. Esta revisión aborda la evolución de los ritmos biológicos, cuya funcionalidad juega un papel clave en la adaptabilidad y el éxito de las especies en respuesta a los patrones externos cambiantes de nuestro planeta.
Abstract
Biological rhythms are a fundamental part of the life of organisms and are closely related to geological movements and periodic environmental changes, such as temperature, humidity, and light. These biological rhythms have developed over time as an evolutionary response to environmental pressures, leading to the formation of genetic circuits that control biological time and regulate the physiology and behavior of living beings. The perception of light is a key factor in the development of biological rhythms since it provides an external signal to adjust the internal biological clocks of organisms. Photolyases and photo perception mechanisms developed in living beings throughout evolution have allowed adaptation to these signals and the formation of the circadian system, which is responsible for regulating daily and annual biological rhythms. In all living beings, there is a circadian system; in mammals, it is in the suprachiasmatic nucleus. The genetic circuit of the internal clock of organisms must be well established at all levels of the organism, since it is essential to regulate the fundamental behaviors of these, such as feeding, reproduction, or migratory processes. The biological rhythms also play an important role in adapting organisms to different geographical areas and seasonal changes. This review addresses the evolution of biological rhythms, whose functionality plays an important role in the adaptability and success of species in response to the changing external patterns of our planet.
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Farner, D. S., King, J. R., & Parkes, K. C. (1971). Avian biology (Vol. 1, pp. 223–286).
Gwinner, E., & Helm, B. (2003). Circannual and circadian contributions to the timing of avian migration. In P. Berthold, E. Gwinner, & E. Sonnenschein (Eds.), Avian migration (pp. 81–95). https://doi.org/10.1007/978-3-662-05957-9_5
Kumar, V., Wingfield, J. C., Dawson, A., Ramenofsky, M., Rani, S., & Bartell, P. (2010). Biological clocks and regulation of seasonal reproduction and migration in birds. Physio-logical and Biochemical Zo-ology, 83(5), 827–835. https://doi.org/10.1086/652243
Postberg, J., Lipps, H. J., & Cremer, T. (2010). Evolutionary origin of the cell nu-cleus and its functional architecture. Es-says in Biochemistry, 48(1), 1–24. https://doi.org/10.1042/BSE0480001
Beckstead, A. A., Zhang, Y., De Vries, M. S., & Kohler, B. (2016). Life in the light: Nu-cleic acid photoproperties as a legacy of chem-ical evolution. Physical Chemistry Chemi-cal Physics, 18(35), 24228–24238. https://doi.org/10.1039/C6CP04230A
Burgess, S. D., Bowring, S., & Shen, S. Z. (2014). High-precision timeline for Earth’s most severe extinction. Proceedings of the National Academy of Sciences of the United States of America, 111(9), 3316–3321. https://doi.org/10.1073/pnas.1317692111
Williams, G. E. (2000). Geological con-straints on the Precambrian history of Earth’s rotation and the Moon’s orbit. Re-views of Geophysics, 38(1), 37–59. https://doi.org/10.1029/1999RG900016
Hill, H. G. M., & Nuth, J. A. (2003). The cata-lytic potential of cosmic dust: Implica-tions for prebiotic chemistry in the solar nebula and other protoplanetary sys-tems. Astrobiology, 3(2), 291–304. https://doi.org/10.1089/153110703769016389
Lissauer, J. J., & De Pater, I. (2019). Funda-mental planetary sciences: Physics, chem-istry and habitability (pp. 1–604). https://doi.org/10.1017/9781108304061
Parker, E. T., Cleaves, H. J., Dworkin, J. P., Glavin, D. P., Callahan, M., Aubrey, A., Lazcano, A., & Bada, J. L. (2011). Primordial synthesis of amines and amino acids in a 1958 Miller H2S-rich spark discharge ex-periment. Proceedings of the National Academy of Sciences of the United States of America, 108(14), 5526–5531. https://doi.org/10.1073/pnas.1019191108
Krishnakumar, S., Gaudana, S. B., Viswana-than, G. A., Pakrasi, H. B., & Wangikar, P. P. (2013). Rhythm of carbon and nitrogen fixation in unicellular cyanobacteria un-der turbu-lent and highly aerobic condi-tions. Biotechnology and Bioengineering, 110(9), 2371–2379. https://doi.org/10.1002/bit.24882
Snape, J. F., Nemchin, A. A., Bellucci, J. J., Whitehouse, M. J., Tartèse, R., Barnes, J. J., Anand, M., Crawford, I. A., & Joy, K. H. (2016). Lunar basalt chronology, mantle differentiation and implications for de-termining the age of the Moon. Earth and Planetary Science Letters, 451, 149–158. https://doi.org/10.1016/j.epsl.2016.07.026
James, K. (1993). Earth’s early atmosphere. Science, 259(5095), 920–927. https://www.jstor.org/stable/2880609
Towe, K. M. (1996). Environmental oxygen conditions during the origin and early evolution of life. Advances in Space Re-search, 18(12), 7–15. https://doi.org/10.1016/0273-1177(96)00022-1
Cockell, C. S. (2000). Ultraviolet radiation and the photobiology of Earth’s early oceans. Origins of Life and Evolution of the Biosphere, 30(5), 467–500. https://doi.org/10.1023/A:1006765405786
Cardona, T., Sánchez-Baracaldo, P., Ruth-erford, A. W., & Larkum, A. W. (2019). Early Archean origin of Photosystem II. Geobi-ology, 17(2), 127–150. https://doi.org/10.1111/gbi.12322
Des Marais, D. J. (2000). When did photo-synthesis emerge on Earth? Science, 289(5485), 1703–1705. https://doi.org/10.1126/science.289.5485.1703
Grotzinger, J. R., & Knoll, A. H. (1999). Stromatolites in Precambrian carbonates: Evolutionary mileposts or environmental dipsticks? Annual Review of Earth and Planetary Sciences, 27, 313–358. https://doi.org/10.1146/annurev.earth.27.1.313
Allwood, A. C., Rosing, M. T., Flannery, D. T., Hurowitz, J. A., & Heirwegh, C. M. (2018). Reassessing evidence of life in 3,700-million-year-old rocks of Greenland. Nature, 565(7737), E1. https://doi.org/10.1038/s41586-018-0759-x
Andújar, C., Arribas, P., & Vogler, A. P. (2017). Terra incognita of soil biodiversity: Un-seen invasions under our feet. Mole-cular Ecology, 26(12), 3087–3089. https://doi.org/10.1111/mec.14112
Carrasco-Ríos, L. (2009). Efecto de la ra-diación ultravioleta-B en plantas. Idesia (Arica), 27(3), 59–76. https://doi.org/10.4067/S0718-34292009000300009
Rajneesh, Pathak, J., Richa, Häder, D. P., & Sinha, R. P. (2019). Impacts of ultraviolet radiation on certain physiological and biochemical processes in cyanobacteria inhabiting di-verse habitats. Environmen-tal and Experimental Botany, 161, 375–387. https://doi.org/10.1016/j.envexpbot.2018.10.037
Vanhaelewyn, L., Van Der Straeten, D., De Coninck, B., & Vandenbussche, F. (2020). Ultraviolet radiation from a plant per-spective: The plant–microorganism con-text. Frontiers in Plant Science, 11, 597642. https://doi.org/10.3389/fpls.2020.597642
Solovchenko, A., & Neverov, K. (2017). Ca-rotenogenic response in photosynthetic organisms: A colorful story. Photosynthe-sis Research, 133(1–3), 31–47. https://doi.org/10.1007/s11120-017-0358-y
Gill, S. S., Anjum, N. A., Gill, R., Jha, M., & Tuteja, N. (2015). DNA damage and repair in plants under ultraviolet and ionizing radiations. ScientificWorldJournal, 2015, 250158. https://doi.org/10.1155/2015/250158.
Karam, P. A., & Leslie, S. A. (2005). Changes in terrestrial natural radiation levels over the history of life. Radioactivity in the En-vironment, 7, 107–117. https://doi.org/10.1016/S1569-4860(04)07011-1
Hays, G. C., Kennedy, H., & Frost, B. W. (2001). Individual variability in diel verti-cal migration of a marine copepod: Why some individuals remain at depth when others mi-grate. Limnology and Oceanog-raphy, 46(8), 2050–2054. https://doi.org/10.4319/lo.2001.46.8.2050
Ringelberg, J. (1999). The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Bio-logical Reviews, 74(4), 397–423. https://doi.org/10.1111/j.1469-185x.1999.tb00036.x
Lo, W. T., Shih, C. T., & Hwang, J. S. (2004). Diel vertical migration of the planktonic copepods at an upwelling station north of Taiwan, western North Pacific. Journal of Plankton Research, 26(1), 89–97. https://doi.org/10.1093/plankt/fbh004
Gehring, W., & Rosbash, M. (2003). The coevolution of blue-light photoreception and circadian rhythms. Journal of Molecu-lar Evolution, 57(Suppl. 1), S286–S289. https://doi.org/10.1007/s00239-003-0038-8
Williamson, C. E., Fischer, J. M., Bollens, S. M., Overholt, E. P., & Breckenridge, J. K. (2011). Toward a more comprehensive theory of zooplankton diel vertical migra-tion: Inte-grating ultraviolet radiation and water transparency into the biotic paradigm. Limnology and Oceanography, 56(5), 1603–1623. https://doi.org/10.4319/lo.2011.56.5.1603
Hobbs, L., Banas, N. S., Cohen, J. H., Cottier, F. R., Berge, J., & Varpe, Ø. (2021). A marine zooplankton community vertically struc-tured by light across diel to interannual timescales. Biology Letters, 17, 20200810. https://doi.org/10.1098/rsbl.2020.0810
Boden, B. P., & Kampa, E. M. (1967). The influence of natural light on the vertical migrations of an animal community in the sea. Symposia of the Zoological Society of London (Vol. 19, pp. 15–26).
Berge, J., Cottier, F., Last, K. S., Varpe, Ø., Leu, E., Søreide, J., Eiane, K., Falk-Petersen, S., Willis, K., Nygård, H., Vogedes, D., Grif-fiths, C., Johnsen, G., Lorentzen, D., & Bri-erley, A. S. (2009). Diel vertical migration of Arctic zooplankton during the polar night. Biology Letters, 5(1), 69–72. https://doi.org/10.1098/rsbl.2008.0484
Grenvald, J. C., Callesen, T. A., Daase, M., Hobbs, L., Darnis, G., Renaud, P. E., Cottier, F., Nielsen, T. G., & Berge, J. (2016). Plank-ton community composition and vertical migration during polar night in Kongs-fjorden. Polar Biology, 39(10), 1879–1895. https://doi.org/10.1007/s00300-016-2015-x
Häder, D.-P. (2022). Solar UV-B and primary producers in aquatic ecosystems. In D.-P. Häder & C. E. Williamson (Eds.), Aquatic ecosystems and UV radiation (pp. 71–92). Springer. https://doi.org/10.1007/978-981-19-3620-3_5
Post, A. F., Eijgenraam, F., & Mur, L. R. (1985). Influence of light period length on photosynthesis and synchronous growth of the green alga Scenedesmus protuber-ans. British Phycological Journal, 20(4), 391–397. https://doi.org/10.1080/00071618500650401
Leach, T. H., Williamson, C. E., Theodore, N., Fischer, J. M., & Olson, M. H. (2015). The role of ultraviolet radiation in the diel vertical migration of zooplankton: An ex-perimental test of the transparency-regulator hypothesis. Journal of Plankton Research, 37(5), 886–896. https://doi.org/10.1093/plankt/fbv061
Pittendrigh, C. S., Kyner, W. T., & Takamu-ra, T. (1991). The amplitude of circadian oscillations: Temperature dependence, latitudinal clines, and the photoperiodic time measurement. Journal of Biological Rhythms, 6(4), 299–313. https://doi.org/10.1177/074873049100600402
Lampert, W. (1993). Ultimate causes of diel vertical migration of zooplankton: New evidence for the predator-avoidance hy-pothesis. Archiv für Hydrobiologie. Bei-heft Ergebnisse der Limnologie, 39, 79–88. https://hdl.handle.net/11858/00-001M-0000-000F-E419-7
Lim, Y. K., Kim, J. H., Ro, H., & Baek, S. H. (2022). Thermotaxic diel vertical migration of the harmful dinoflagellate Cochlodini-um (Margalefidinium) polykrikoides: Combined field and laboratory studies. Harmful Algae, 118, 102315. https://doi.org/10.1016/j.hal.2022.102315
Sancar, A. (2003). Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chemical Re-views, 103(6), 2203–2237. https://doi.org/10.1021/cr0204348
Todo, T., Ryo, H., Yamamoto, K., Toh, H., Inui, T., Ayaki, H., Nomura, T., & Ikenaga, M. (1996). Similarity among the Drosophila (6-4) photolyase, a human photolyase homolog, and the DNA photolyase-blue-light photoreceptor family. Science, 272(5258), 109–112. https://doi.org/10.1126/science.272.5258.109
Deppisch, P., Helfrich-Förster, C., & Senthilan, P. R. (2022). The gain and loss of Cryptochrome/Photolyase family mem-bers during evolution. Genes, 13(9), 1613. https://doi.org/10.3390/genes13091613
Devlin, P. F., & Kay, S. A. (2000). Crypto-chromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. The Plant Cell, 12(12), 2499–2509. https://doi.org/10.1105/tpc.12.12.2499
Emery, P., Stanewsky, R., Hall, J. C., & Rosbash, M. (2000). Drosophila crypto-chromes: A unique circadian-rhythm pho-toreceptor. Nature, 404(6777), 456–458. https://doi.org/10.1038/35006558
Okano, S., Kanno, S. I., Takao, M., Eker, A. P. M., Isono, K., Tsukahara, Y., & Yasui, A. (1999). A putative blue-light receptor from Drosophila melanogaster. Photochemis-try and Photobiology, 69(1), 108–113. https://doi.org/10.1111/j.1751-1097.1999.tb05314.x
Cashmore, A. R. (2003). Cryptochromes: Enabling plants and animals to deter-mine circadian time. Cell, 114(5), 537–543. https://doi.org/10.1016/j.cell.2003.08.004
Gehring, W., & Rosbash, M. (2003). The coevolution of blue-light photoreception and circadian rhythms. Journal of Molecu-lar Evolution, 57(Suppl 1), S286–S289. https://doi.org/10.1007/s00239-003-0038-8
Partch, C. L., Green, C. B., & Takahashi, J. S. (2014). Molecular architecture of the mammalian circadian clock. Trends in Cell Biology, 24(2), 90–99. https://doi.org/10.1016/j.tcb.2013.07.002
Friedrich, M. (2006). Ancient mechanisms of visual sense organ development based on comparison of the gene networks con-trolling larval eye, ocellus, and compound eye specification in Drosophila. Arthro-pod Structure & Development, 35(4), 357–378. https://doi.org/10.1016/j.asd.2006.08.010
Gehring, W. J. (2004). Historical perspec-tive on the development and evolution of eyes and photoreceptors. The Interna-tional Journal of Developmental Biology, 48(8–9), 707–717. https://doi.org/10.1387/ijdb.041900wg
Casal, J. J. (2000). Phytochromes, crypto-chromes, phototropin: Photoreceptor in-teractions in plants. Photochemistry and Photobiology, 71(1), 1–11. https://doi.org/10.1562/0031-8655(2000)071<0001:PCPPII>2.0.CO;2
Armitage, J. P., & Hellingwerf, K. J. (2003). Light-induced behavioral responses ("photo-taxis") in prokaryotes. Photosyn-thesis Research, 76(1–3), 145–155. https://doi.org/10.1023/a:1024974111818
Jékely, G. (2009). Evolution of phototaxis. Philosophical Transactions of the Royal Socie-ty B: Biological Sciences, 364(1531), 2795–2808. https://doi.org/10.1098/rstb.2009.0072
Guido, M. E., Marchese, N. A., Rios, M. N., Morera, L. P., Diaz, N. M., Garbarino-Pico, E., & Contin, M. A. (2020). Non-visual op-sins and novel photodetectors in the ver-tebrate inner retina mediate light re-sponses within the blue spectrum region. Cellular and Molecular Neurobiology, 42(1), 59–83. https://doi.org/10.1007/s10571-020-00997-x
Lamb, T. D. (2022). Photoreceptor physiol-ogy and evolution: Cellular and molecular basis of rod and cone phototransduction. The Journal of Physiology, 600(21), 4585–4601. https://doi.org/10.1113/JP282058
Kaylor, J. J., Frederiksen, R., Bedrosian, C. K., Huang, M., Stennis-Weatherspoon, D., Huynh, T., Ngan, T., Mulamreddy, V., Sam-path, A. P., Fain, G. L., & Travis, G. H. (2024). RDH12 allows cone photoreceptors to re-generate opsin visual pigments from a chromophore precursor to escape com-petition with rods. Current Biology, 34(15), 3342–3353.e6. https://doi.org/10.1016/j.cub.2024.06.031
Yamaguchi, Y., et al. (2025). Pivotal roles of melanopsin-containing retinal ganglion cells in pupillary light reflex in photopic conditions. Frontiers in Cellular Neuro-science, 15, 1547066. https://doi.org/10.3389/fncel.2025.1547066
Stanewsky, R., Kaneko, M., Emery, P., Beretta, B., Wager-Smith, K., Kay, S. A., Rosbash, M., & Hall, J. C. (1998). The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell, 95(5), 681–692. https://doi.org/10.1016/s0092-8674(00)81638-4
He, Y., Yu, Y., Wang, X., Qin, Y., & Su, C. (2022). Aschoff's rule on circadian rhythms orchestrated by blue light sensor CRY2 and clock component PRR9. Nature Com-munications, 13, 5923. https://doi.org/10.1038/s41467-022-33617-7
Green, C. B. (2023). Cryptochromes: Blue light photoreceptors in plants and ani-mals. Annual Review of Plant Biology, 74, 123–146. https://doi.org/10.1146/annurev-arplant-102322-045123
Goity, A., Dovzhenok, A., Lim, S., Hong, C., Loros, J., Dunlap, J. C., & Larrondo, L. F. (2024). Transcriptional rewiring of an evo-lutionarily conserved circadian clock. The EM-BO Journal, 43(10), 2015–2034. https://doi.org/10.1038/s44318-024-00088-3.
Hut, R. A., & Beersma, D. G. M. (2023). Step in time: Conservation of circadian clock genes in animal evolution. Integrative and Comparative Biology, 63(1), 1–15. https://doi.org/10.1093/icb/icac099
Lowrey, P. L., & Takahashi, J. S. (2004). Mammalian circadian biology: Elucidating genome-wide levels of temporal organi-zation. Annual Review of Genomics and Human Genetics, 5, 407–441. https://doi.org/10.1146/annurev.genom.5.061903.175925
Ko, C. H., & Takahashi, J. S. (2006). Molecu-lar components of the mammalian circa-dian clock. Human Molecular Genetics, 15(Suppl 2), R271–R277. https://doi.org/10.1093/hmg/ddl207
Kang, T. H., Lindsey-Boltz, L. A., Reardon, J. T., & Sancar, A. (2010). Circadian control of XPA and excision repair of cisplatin-DNA damage by cryptochrome and HERC2 ubiquitin ligase. Proceedings of the Na-tional Academy of Sciences, 107(11), 4890–4895. https://doi.org/10.1073/pnas.0915085107
Lin, J. M., Kilman, V. L., Keegan, K., Pad-dock, B., Emery-Le, M., Rosbash, M., & Al-lada, R. (2002). A role for casein kinase 2α in the Drosophila circadian clock. Nature, 420(6917), 816–820. https://doi.org/10.1038/nature01235
Reppert, S. M., & Weaver, D. R. (2002). Co-ordination of circadian timing in mam-mals. Nature, 418(6901), 935–941. https://doi.org/10.1038/nature00965
Buijs, R. M., Salgado, R., Sabath, E., & Es-cobar, C. (2013). Peripheral circadianoscil-lators: Time and food. In C. A. C. (Ed.), Pro-gress in Molecular Biology and Transla-tional Science (Vol. 119, pp. 83–103). Else-vier. https://doi.org/10.1016/B978-0-12-396971-2.00004-X
Moore, R. Y., Speh, J. C., & Leak, R. K. (2002). Suprachiasmatic nucleus organization. Cell and Tissue Research, 309(1), 89–98. https://doi.org/10.1007/s00441-002-0575-2
Lu, Q., & Kim, J. Y. (2022). Mammalian cir-cadian networks mediated by the supra-chias-matic nucleus. The FEBS Journal, 289(21), 6589–6604. https://doi.org/10.1111/febs.16233
Kume, K., Zylka, M. J., Sriram, S., Shearman, L. P., Weaver, D. R., Jin, X., Maywood, E. S., Hastings, M. H., & Reppert, S. M. (1999). mCRY1 and mCRY2 are essential com-ponents of the negative limb of the circa-dian clock feedback loop. Cell, 98(2), 193–205. https://doi.org/10.1016/s0092-8674(00)81014-4
Shearman, L. P., Jin, X., Lee, C., Reppert, S. M., & Weaver, D. R. (2000). Targeted dis-ruption of the mPer3 gene: Subtle effects on circadian clock function. Molecular and Cellular Biology, 20(17), 6269–6275. https://doi.org/10.1128/mcb.20.17.6269-6275.2000
Marri, D., Filipovic, D., Kana, O., Tischkau, S., & Bhattacharya, S. (2023). Prediction of mammalian tissue-specific CLOCK-BMAL1 binding to E-box DNA motifs. Scientific Re-ports, 13, 7742. https://doi.org/10.1038/s41598-023-34115-w
Dibner, C., Schibler, U., & Albrecht, U. (2010). The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annual Re-view of Physio-logy, 72, 517–549. https://doi.org/10.1146/annurev-physiol-021909-135821
Moore, R. Y., & Lenn, N. J. (1972). A retino-hypothalamic projection in the rat. The Journal of Comparative Neurology, 146(1), 1–14. https://doi.org/10.1002/cne.901460102
Toledo, R., Aguilar-Roblero, R., Canchola, E., & Caba, M. (2004). Tracto retinohipotá-la-mico en el conejo. Universidad y Cien-cia, 20(40), 55–60. https://www.redalyc.org/articulo.oa?id=15404002
Liu, A. C., Welsh, D. K., Ko, C. H., Tran, H. G., Zhang, E. E., Priest, A. A., Buhr, E. D., Singer, O., Meeker, K., Verma, I. M., Doyle, F. J., Ta-kahashi, J. S., & Kay, S. A. (2007). Intercellu-lar coupling confers robustness against mutations in the SCN circadian clock net-work. Cell, 129(3), 605–616. https://doi.org/10.1016/j.cell.2007.02.047
Saini, C., Morf, J., Stratmann, M., Gos, P., & Schibler, U. (2012). Simulated body tem-perature rhythms reveal the phase-shifting behavior and plasticity of mam-malian circadian oscillators. Genes & De-velopment, 26(6), 567–580. https://doi.org/10.1101/gad.183251.111
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