Journal Article

Circadian Rhythms of Embryonic Development and Hatching in Fish: A Comparative Study of Zebrafish (Diurnal), Senegalese Sole (Nocturnal), and Somalian Cavefish (Blind)

Villamizar, N., Blanco-Vives, B., Oliveira, C., Dinis, M.T., Di Rosa, V., Negrini, P., Bertolucci, C. and Sanchez-Vazquez, F.J.

Record Number:
3010
Year:
2013
Journal:
Chronobiology International
Pages:
889-900
Volume:
30
Abstract:
During early development, most organisms display rhythmic physiological processes that are shaped by daily changes in their surrounding environment (i.e., light and temperature cycles). In fish, the effects of daily photocycles and their interaction with temperature during early developmental stages remain largely unexplored. We investigated the existence of circadian rhythms in embryonic development and hatching of three teleost species with different daily patterns of behavior: diurnal (zebrafish), nocturnal (Senegalese sole), and blind, not entrained by light (Somalian cavefish). To this end, fertilized eggs were exposed to three light regimes: 12 h of light: 12 h of darkness cycle (LD), continuous light (LL), or continuous darkness (DD); and three species-appropriate temperature treatments: 24 degrees C, 28 degrees C, or 32 degrees C for zebrafish and cavefish and 18 degrees C, 21 degrees C, or 24 degrees C for sole. The results pointed to the existence of daily rhythms of embryonic development and hatching synchronized to the LD cycle, with different acrophases, depending on the species: zebrafish embryos advanced their developmental stage during the light phase, whereas sole did so during the dark phase. In cavefish, embryogenesis occurred within 24 h post fertilization (hpf) at the same pace during day or night. The hatching rhythms appeared to be controlled by a clock mechanism that restricted or "gated" hatching to a particular time of day/night (window), so that embryos that reached a certain developmental state by that time hatch, whereas those that have not wait until the next available window. Under LL and DD conditions, hatching rhythms and the gating phenomenon persisted in cavefish, in zebrafish they split into ultradian bouts of hatching occurring at 12-18-h intervals, whereas in sole DD and LL produced a 24-h delay and advance, respectively. Hatching rates were best under the LD cycle and the reported optimal temperature for each species (95.2 +/- 2.7% of the zebrafish and 83.3 +/- 0.1% of the cavefish embryos hatched at 28 degrees C, and 93.1 +/- 2.9% of the sole embryos hatched at 21 degrees C). In summary, these results revealed that hatching rhythms in fish are endogenously driven by a time-keeping mechanism, so that the day and time of hatching are determined by the interplay between the developmental state (temperature-sensitive) and the circadian clock (temperature-compensated), with the particular phasing being determined by the diurnal/nocturnal behavior of the species.
Times Cited:
1
Related Records:
Pellegrin, J. (1931)
Les Cyprinides cavernicoles d'Afrique
Parenzan, P. (1939)
Pesci del acque sotterranee della Somalia
Ercolini, A. and Berti, R. (1975)
Light sensitivity experiments and morphology studies of the blind phreatic fish Phreatichthys andruzzii from Somalia
Bianchi, S. (1978)
Osservazioni preliminari sulle cellule mucose di Phreatichthys andruzzii Vinciguerra, pesce freatico anoftalmo della Somalia
Messana, G. (1979)
Groundwater research by the "Centro di studio par la faunistica ed ecologia tropicali" in Somalia
Delfino, G., Bianchi, S. and Ercolini, A. (1981)
On the olfactory epithelium in cyprinids: A comparison between hypogean and epigean species
Andreoli, C. (1981)
La flora algale presente in due particolari pozzi della Somalia meridionale
Berti, R., Thines, G. and Lefevre, B. (1982)
Effets des informations chimiques provenant d'un milieu habite par des congeneres sur l'orientation topographique du poisson cavernicole Phreatichthys andruzzii Vinciguerra (Pisces, Cyprinidae)
Ercolini, A., Berti, R., Chelazzi, L. and Messana, G. (1982)
Researches on the phreatobitic fishes of Somalia: Acheivements and prospects
Leveque, C. and Daget, J. (1984)
Phreatichthys anduzzii Vinciguerra, 1924
Messana, G., Chelazzi, L. and Baccetti, N. (1985)
Biospeleology of Somalia: Mugdile and Showli Berdi caves
Messana, G. and Chelazzi, L. (1986)
The fauna of the subterranean waters of East Africa, and particularly of Somalia
Ercolini, A., Berti, R., Chelazzi, L. and Messana, G. (1987)
Oxygen consumption in hypogean and epigean cyprinids (Pisces)
Berti, R. (1990)
Specific chemical recognition in Phreatichthys andruzzii (Pisces, Cyprinidae)
Berti, R. and Masciarelli, L. (1993)
Comparative performances of non-visual food search in the hypogean cyprinid Phreatichthys andruzzii and the epigean relative Barbus filamentosus
Sbordoni, M. C., Dematthaeis, E., Mattoccia, M., Berti, R. and Sbordoni, V. (1996)
Genetic variability and differentiation of hypogean cyprinid fishes from Somalia
Frangioni, G., Berti, R. and Borgioli, G. (1997)
Hepatic respiratory compensation and haematological changes in the cave cyprinid, Phreatichthys andruzzii
Berti, R and Zorn, L. (2001)
Locomotory responses of the cave cyprinid Phreatichthys andruzzii to chemical signals from conspecifics abd related species: new findings
Berti, R., Durand, J., Becchi, S., Brizzi, R., Keller, N. and Ruffat, G. (2001)
Eye degeneration in the blind cave-dwelling fish Phreatichthys andruzzii
Janiaud, D and Berti, R (2001)
Phototactic response of juveniles of the cave cyprinid Phreatichthys andruzzii
Trabalzini, G, Janiaud, D and Berti, R (2001)
Alarm substance and fright reaction in the cave cyprinid Phreatichthys andruzzii
Messana, G. (2001)
Somalia
Aden, E. (2002)
Eye regression in the cavefish Phreatichthys andruzzii
Thieme, M.L., Abell, R., Stiassny, M.L.J.,Skelton, P., Lehner, B., Teugels, G., Dinerstein, E., Kamdem-Toham, A., Burgess, B., and Olson, D. (2005)
Freshwater ecoregions of Africa and Madagascar. A conservation assessment
Brown, A. and Thieme, M. (2005)
Ecoregion 83. Horn
Colli, L., Berti, R., Marzano, F.N., Gandolfi, G. and Tagliavini, J. (2006)
Collocazione sistematica del ciprinide ipogeo Phreatichthys andruzzii Vinciguerra, 1924: considerazioni filogenetiche e biogeographiche
Paglianti, A, Messana, G, Cianfanelli, A and Berti, R (2006)
Is the perception of their own odour effective in orienting the exploratory activity of cave fishes?
Aden, E. (2008)
Ontogenetic and phylogenetic aspects of regression processes in cave fish: immunohistochemical studies on the blind fish Phreatichthys andruzzii Vinciguerra, 1924
Colli, L., Paglianti, A., Berti, R., Gandolfi, G. and Tagliavini, J. (2009)
Molecular phylogeny of the blind cavefish Phreatichthys andruzzii and Garra barreimiae within the family Cyprinidae
Dezfuli, B.S., Capuano, S., Magosso, S., Giari, L. and Berti, R. (2009)
The lateral line system in larvae of the blind Cyprinid cavefish, Phreatichthys andruzzii
Dezfuli, B.S., Magosso, S., Simoni, E., Hills, K. and Berti, R. (2009)
Ultrastructure and Distribution of Superficial Neuromasts of Blind Cavefish, Phreatichthys andruzzii, Juveniles
Sguanci, S., Ceccolini, F. and Berti, R. (2010)
Non visual discrimination of shapes in the blind cave cyprinid Phreatichthys andruzzii Vinciguerra 1924
Ceccolini, F., Paglianti, A, Streitenberger, C. and Berti, R. (2010)
Can chemical cues act as landmarks in the orientation of the cavefish Phreatichthys andruzzii?
Berti, R. and Messana, G. (2010)
Subterranean fishes of Africa
Cavallari, N., Frigato, E., Vallone, D., Froehlich, N., Lopez-Olmeda, J.F., Foa, A., Berti, R., Sanchez-Vazquez, F.J., Bertolucci, C. and Foulkes, N.S. (2011)
A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception
Tarttelin, E.E., Frigato, E., Bellingham, J., Di Rosa, V., Berti, R., Foulkes, N.S., Lucas, R.J. and Bertolucci, C. (2012)
Encephalic photoreception and phototactic response in the troglobiont Somalian blind cavefish Phreatichthys andruzzii
Idda, M.L., Bertolucci, C., Vallone, D., Gothilf, Y., Sánchez-Vázquez, F.J. and Foulkes N.S. (2012)
Circadian clocks: lessons from fish
Stemmer, M., Schuhmacher, L.-N., Foulkes, N.S., Bertolucci, C. and Wittbrodt, J. (2013)
Unravelling continuous eye growth in teleosts by studying blind cavefish
Villamizar, N., Blanco-Vives, B., Oliveira, C., Dinis, M.T., Di Rosa, V., Negrini, P., Bertolucci, C. and Sanchez-Vazquez, F.J. (2013)
Circadian Rhythms of Embryonic Development and Hatching in Fish: A Comparative Study of Zebrafish (Diurnal), Senegalese Sole (Nocturnal), and Somalian Cavefish (Blind)
Bisazza, A., Tagliapietra, C., Bertolucci, C., Foa, A. and Agrillo, C. (2014)
Non-visual numerical discrimination in a blind cavefish (Phreatichthys andruzzii)
Stemmer, M., Schuhmacher, L.-N., Foulkes, N.S., Bertolucci, C. and Wittbrodt, J. (2015)
Cavefish eye loss in response to an early block in retinal differentiation progression
Negrini, P. (2015)
Molecular and bioinformatic analysis of the circadian clock in Phreatichthys andruzzii
Sayyadzadeh, G., Esmaeili, H.R. and Freyhof, J. (2015)
Garra mondica, a new species from the Mond River drainage with remarks on the genus Garra from the Persian Gulf basin in Iran
Esmaeili, H.R., Sayyadzadeh, G., Coad, B.W. and Eagderi, S. (2016)
Review of the genus Garra Hamilton, 1822 in Iran with description of a new species: a morpho-molecular approach (Teleostei: Cyprinidae)
Bagheri, M., Goudarzi, F., Zalaghi, A.H. and Savabieasfahani, M. (2016)
Habitat characteristics and population size of Iranocypris typhlops, the Iran cave barb
Foulkes, N.S., Whitmore, D., Vallone, D and Bertolucci, C. (2016)
Studying the evolution of the vertebrate circadian clock: The power of fish as compataive models
Calderoni, L., Rota-Stabelli, O., Frigato, E., Panziera, A., Lirchner, S., Foulkes, N.S., Kruckenhauser, L., Bertolucci, C. and Fuselli, S. (2016)
Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonisation
Laumanns, M. (2017)
Atlas of the Great caves and the karst of Africa. Volume 2. Malawi to Zimbabwe and general references
Nebeshwar, K and Vishwanath, W (2017)
On the snout and oromandibular morphology of genus Garra, description of two new species from the Koladyne River basin in Mizoram, India, and redescription of G. manipurensis (Teleostei: Cyprinidae)
Malek-Hosseini, M.J. and Zamani, A. (2017)
A checklist of subterranean arthropods of Iran
Esmaeili, H.R., Mehraban, H., Abbasi, K., Keivany, Y. and Coad, B. (2017)
Review and updated checklist of freshwater fishes of Iran: Taxonomy, distribution and conservation status
Grandi, G, Pezzi, M, Marchetti, MG and Chicca, M (2017)
Immunocytochemical identification and ontogeny of adenohypophyseal cells in a cave fish, Phreatichthys andruzzii (Cypriniformes: Cyprinidae)
Ceinos, R., Frigato, E., Pagano, C., Fröhlich, N., Negrini, P., Cavallari, N., Vallone, D., Fuselli, S., Bertolucci, C. and Foulkes, N. (2018)
Mutations in blind cavefish target the light-regulated circadian clock gene, period 2
Pagano, C., Siauciunaite, R., Idda, M.L., Ruggiero, G., Ceinos, R.M., Pagano, M., Frigato, E., Bertolucci, C., Foulkes, N.S. and Vallone, D. (2018)
Evolution shapes the responsiveness of the D-box enhancer element to light and reactive oxygen species in vertebrates
Zhao, H., Di Mauro, G., Lungu-Mitea, S., Negrini, P., Guarino, A.M., Frigato, E., Braunbeck, T., Ma, H., Lamparter, T., Vallone, D., Bertolucci, C. and Foulkes, N.S. (2018)
Modulation of DNA repair systems in blind cavefish during evolution in constant darkness
Rohner, N. (2018)
Evolution: A dark past
Sovrano, V.A., Potrich, D., Foà, A. and Bertolucci, C. (2018)
Extra-visual systems in the spatial reorientation of cavefish
Pucci, A., Berti, R. and Simonetta, A. (2019)
The skull osteology of the blind cave cyprinid Phreatichthys andruzzii Vinciguerra, 1924
Saemi-Komsari, M., Mousavi-Sabet, H., Sattari, M., Eagderi, S., Vatandoust, S. and Doadrio, I. (2020)
Descriptive osteology of Garra rossica (Nikolskii 1900)
Zhao, H., Li, H., Du, J., Di Mauro, G., Lungu-Mitea, S., Geyer, N., Vallone, D., Bertolucci, C. and Foulkes, N.S. (2021)
Regulation of ddb2 expression in blind cavefish and zebrafish reveals plasticity in the control of sunlight-induced DNA damage repair
Zamani-Faradonbe, M., Keivany, Y., Dorafshan, S. and Zhang, E. (2021)
Two new species of Garra (Teleostei: Cyprinidae) from western Iran
Zamani-Faradonbe M. and Keivany Y. (2021)
Biodiversity and distribution of Garra species (Teleostei: Cyprinidae) in Iran
Zamani-Faradonbe, M. and Keivany, Y. (2021)
Comparative osteology of two Garra species (Cypriniformes, Cyprinidae) from Hormuz and Sistan basins of Iran
Zamani-Faradonbe, M., Zhang, E. and Keivany, Y. (2021)
Garra hormuzensis, a new species from the upper Kol River drainage in the Persian Gulf basin (Teleostei: Cyprinidae)
Baratti, G., Potrich, D., Lee, S.A., Morandi-Raikova, A. and Sovrano, V.A. (2022)
The geometric world of fishes: A synthesis on spatial reorientation in Teleosts
Pavlova, V.V. and Krylov, V.V. (2023)
Cavefishes in chronobiological research: A narrative review.
Di Rosa, V., Frigato, E., Negrini, P., Cristiano, W., López-Olmeda, J.F., Rétaux, S., Sánchez-Vázquez, F.J., Foulkes, N.S., Bertolucci, C. (2024)
Sporadic feeding regulates robust food entrainable circadian clocks in blind cavefish
Keene, A.C., Duboue, E.R., Foulkes, N.S. and Bertolucci, C. (2024)
Evolved loss of sleep and circadian rhythms in cavefish
Rétaux, S. and Yamamoto, K. (2024)
Evolution of fish brains and behaviors: how many ways to generate the same outcomes?