Conservation of the photoperiodic neuroendocrine axis among vertebrates: Evidence from the teleost fish, Gasterosteus aculeatus

General and Comparative Endocrinology

Volumn 178, Issue 1, 2012, Pages 19-27

  O'Brien, Conor S ^a   Bourdo, Ryan ^a   Bradshaw, William E ^a   Holzapfel, Christina M ^a   Cresko, William A ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Gonadotropin releasing hormone; Lutenizing hormone; Photoperiodism; Threespine stickleback; Thyroid hormone; Thyroid stimulating hormone

Indexed keywords

GONADORELIN; LUTEINIZING HORMONE; THYROTROPIN; THYROTROPIN BETA1; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLIMATE; CONTROLLED STUDY; GASTEROSTEUS ACULEATUS; GENE EXPRESSION; HYPOPHYSIS PARS DISTALIS; NEUROENDOCRINE SYSTEM; NONHUMAN; PHOTOPERIODICITY; PRIORITY JOURNAL; SEXUAL MATURATION; TELEOST;

EID: 84860290317     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.03.010     Document Type: Article

References (67)

1. Akaike H. Information theory and an extension of the maximum likelihood principle. Proceedings of the Second International Symposium on Information Theory 1973, 267-281. Akademiai Kiado, Budapest. B.H. Petrov, F. Caski (Eds.).
2. Amano M., Ikuta K., Kitamura S., Aida K. Effects of photoperiod on salmon GnRH mRNA levels in brain of castrated underyearling precocious male masu salmon. Gen. Comp. Endocrinol. 1999, 115:70-75.
3. Amano M., Ikuta K., Kitamura S., Aida K. Effects of photoperiod on pituitary gonadotropin levels in masu salmon. J. Exp. Zool. 2001, 289:449-455.
4. Andersson E., Bogerd J., Borg B., Sharp P.J., Sherwood N.M., Goos H.J.T. Characterization and localization of gonadotropin-releasing hormone in the brain and pituitary of the three-spined stickleback. Gasterosteus aculeatus, Cell Tissue Res. 1995, 279:485-493.
5. Anisimova M., Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Sys. Biol. 2006, 55:539-552.
6. Baggerman B. The roles of daily and annual biological rhythms in the photoperiodic regulation of the breeding season in the stickleback Gasterosteus aculeatus L. Behav. 1985, 93:1-7.
7. Biswas A., Kundu S., Roy S., De J., Pramanik M., Ray A.K. Thyroid hormone profile during annual reproductive cycle of diploid and triploid catfish, Heteropneustes fossilis (Bloch). Gen. Comp. Endocrinol. 2006, 147:126-132.
8. Borg B. Photoperiodism in fishes. Photoperiodism: the Biological Calendar 2010, 371-398. Oxford University Press, New York. R.J. Nelson, D.L. Denlinger, D.E. Somers (Eds.).
9. Borg B., Bornestaf C., Hellqvist A., Schmitz M., Mayer I. Mechanisms in the photoperiodic control of reproduction in the stickleback. Behav. 2004, 131:1521-1530.
10. Bradshaw W.E., Holzapfel C.M. Evolution of animal photoperiodism. Annu. Rev. Ecol. Evol. Syst. 2007, 38:1-25.
11. Bradshaw W.E., Holzapfel C.M. Light, time, and the physiology of biotic response to rapid climate change in animals. Annu. Rev. Physiol. 2010, 72:147-166.
12. Bradshaw W.E., Zani P.A., Holzapfel C.M. Adaptation to temperate climates. Evol. 2004, 58:1748-1762.
13. Bromage N., Porter M., Randall C. The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquac. 2001, 197:63-98.
14. Cassone V. Melatonin's role in vertebrate circadian rhythms. Chronobiol. Int. 1998, 15:457-473.
15. Catchen J.M., Braasch I., Postlethwait J.H. Conserved synteny and the zebrafish genome. The Zebrafish: Genetics, Genomics, and Informatics 2011, 256-268. Elsevier Science, Amsterdam. W.H. Dietrich, M. Westerfield, L.I. Zon (Eds.).
16. Catchen J.M., Conery J.M., Postlethwait J.H. Automated identification of conserved synteny after whole-genome duplication. Genome Res. 2009, 19:1497-1505.
17. Cerdá-Reverter J.M., Canosa L.F. Anatomical neuroendocrinology. Fish Physiology 2009, 4-55. Elsevier Science, Netherlands. N.J. Bernier, G. Van Der Kraak, P. Anthony, C.J. Brauner (Eds.).
18. Chen C.C., Fernald R.D. GnRH and GnRH receptors: distribution, function and evolution. J. Fish Biol. 2008, 73:1099-1120.
19. Choi S., Lee C.H., Park W., Kim D.J., Sohn Y.C. Effects of shortened photoperiod on gonadotropin-releasing hormone, gonadotropin, and vitellogenin gene expression associated with ovarian maturation in rainbow trout. Zool. Sci. 2010, 27:24-32.
20. Cyr D.G., Bromage N.R., Duston J., Eales J.G. Seasonal patterns in serum levels of thyroid hormones and sex steroids in relation to photoperiod-induced changes in spawning time in rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 1988, 69:217-225.
21. Cyr D.G., Eales J.G. Interrelationships between thyroidal and reproductive endocrine systems in fish. Rev. Fish Biol. Fish. 1996, 6:165-200.
22. Dardente H., Wyse C.A., Birnie M.J., Dupré S.M., Loudon A.S., Lincoln G.A., Hazlerigg D.G. A molecular switch for photoperiod responsiveness in mammals. Curr. Biol. 2010, 20:2193-2198.
23. Dawson A. Photoperiodic control of the annual cycle in birds and comparison with mammals. Ardea 2002, 90:355-367.
24. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
25. Finley C.M., Gorman M.R., Tuthill C.R., Zucker I. Long-term reproductive effects of a single long Day in the Siberian hamster (Phodopus sungorus). J. Biol. Rhythm. 1995, 10:33-41.
26. Goldman B.D., Gwinner E., Karsch F.J., Saunders D.S., Zucker I., Gall G.F. Circannual rhythms and photoperiodism. Chronobiology: Biological Timekeeping 2004, 107-142. Sinauer Associates, Sunderland. J.C. Dunlap, J.J. Loros, P.J. DeCoursey (Eds.).
27. Guindon S., Delsuc F., Dufayard J., Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol 2009, 537:113-137.
28. Halford S., Pires S.S., Turton M., Zheng L., Gonzalez-Menéndez I., Davies W.L., Peirson S.N., Garcia-Fernandez J.M., Hankins M.W., Foster R.G. VA opsin-based photoreceptors in the hypothalamus of birds. Curr. Biol. 2009, 19:1396-1402.
29. Hanon E.A., Lincoln G.A., Fustin J.M., Dardente H., Masson-Pévet M., Morgan P.J., Hazlerigg D.G. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr. Biol. 2008, 18:1147-1152.
30. Hellqvist A., Bornestaf C., Borg B., Schmitz M. Cloning and sequencing of the FSH-β and LH β-subunit in the three-spined stickleback, Gasterosteus aculeatus, and effects of photoperiod and temperature on LH-β and FSH-β mRNA expression. Gen. Comp. Endocrinol. 2004, 135:167-174.
31. Hellqvist A., Schmitz M., Mayer I., Borg B. Seasonal changes in expression of LH-β and FSH-β in male and female three-spined stickleback, Gasterosteus aculeatus. Gen. Comp. Endocrinol. 2006, 145:263-269.
32. Heyland A., Hodin J., Reitzel A.M. Hormone signaling in evolution and development: a non-model system approaches. BioEssays 2005, 27:64-75.
33. Hibbeler S., Scharsack J., Becker S. Housekeeping genes for quantitative expression studies in the three-spined stickleback Gasterosteus aculeatus. BMC Mol. Biol. 2008, 9:9-18.
34. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Computer applications in the biosciences: CABIOS 1992, 8:275-282.
35. Kah O., Dufour S. Conserved and divergent features of reproductive neuroendocrinology in teleost fishes. Hormones and Reproduction of Vertebrates 2010, 15-42. Elsevier Press, New York. D.O. Norris, K.H. Lopez (Eds.).
36. Karvé A., von Hippel F., Bell M. Isolation between sympatric anadromous and resident threespine stickleback species in Mud Lake, Alaska. Environ. Biol. Fish. 2008, 81:287-296.
37. Kitano J., Lema S.C., Luckenbach J.A., Mori S., Kawagishi Y., Kusakabe M., Swanson P., Peichel C.L. Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation. Curr. Biol. 2010, 20:2124-2130.
38. C.M. Kuo, C.E. Nash, Z.H. Shehadeh, The effects of temperature and photoperiod on ovarian development in captive grey mullet (Mugil cephalus L.), Aquac. 3 (1974) 25-43.
39. T. Masuda, M. Iigo, K. Aida, Existence of an extra-retinal and extra-pineal photoreceptive organ that regulates photoperiodism in gonadal development of an Osmerid teleost, ayu (Plecoglossus altivelis), Comp. Biochem. Physiol. - Part A: Mol. Integr. Physiol. 140 (2005) 414-422.
40. Masumoto K.H., Ukai-Tadenuma M., Kasukawa T., Nagano M., Uno K.D., Tsujino K., Horikawa K., Shigeyoshi Y., Ueda H.R. Acute induction of eya3 by late-night light stimulation triggers TSHβ expression in photoperiodism. Curr. Biol. 2010, 20:2199-2206.
41. Mayer I., Bornestaf C., Borg B. Melatonin in non-mammalian vertebrates: Physiological role in reproduction?. Comp. Biochem. Physiol. Part A: Physiol. 1997, 118:515-531.
42. Migaud H., Davie A., Taylor J.F. Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J. Fish Biol. 2010, 76:27-68.
43. Miranda L., Strüssmann C., Somoza G. Effects of light and temperature conditions on the expression of GnRH and GtH genes and levels of plasma steroids in Odontesthes bonariensis females. Fish Physiol. Biochem. 2009, 35:101-108.
44. Moore R.Y. Neural control of the pineal gland. Behav. Brain Res. 1995, 73:125-130.
45. Nakane Y., Ikegami K., Ono H., Yamamoto N., Yoshida S., Hirunagi K., Ebihara S., Kubo Y., Yoshimura T. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15264-15268.
46. Nakao N., Ono H., Yamamura T. T Anraku, T. Takagi, K. Higashi, S. Yasuo, Y. Katou, S. Kageyama, Y. Uno, T. Kasukawa, M. Iigo, P.J. Sharp, A. Iwasawa, Y. Suzuki, S. Sugano, T. Niimi, M. Mizutani, T. Namikawa, S. Ebihara, H.R. Ueda, T. Yoshimura, Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 2008, 452:317-322.
47. Nocedal J. Updating quasi-Newton matrices with limited storage. Math. Comput. 1980, 35:773-782.
48. Nocillado J.N., Levavi-Sivan B., Carrick F., Elizur A. Temporal expression of G-protein-coupled receptor 54 (GPR54), gonadotropin-releasing hormones (GnRH), and dopamine receptor D2 (drd2) in pubertal female grey mullet, Mugil cephalus. Gen. Comp. Endocrinol. 2007, 150:278-287.
49. Norberg B., Brown C.L., Halldorsson O., Stensland K., Björnsson B.T. Photoperiod regulates the timing of sexual maturation, spawning, sex steroid and thyroid hormone profiles in the Atlantic cod (Gadus morhua). Aquac. 2004, 229:451-467.
50. C.S. O'Brien, L.A. Unruh, C.E. Zimmerman, W.E. Bradshaw, C.M. Holzapfel, W.A. Cresko, Geography of the circadian gene clock and photoperiodic response in western North American populations of the threespine stickleback, Gasterosteus aculeatus, in prep.
51. Okubo K., Nagahama Y. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol. 2008, 193:3-15.
52. Orozco A., Valverde R.C. Thyroid hormone deiodination in fish. Thyroid 2005, 15:799-813.
53. Parhar I.S., Soga T., Sakuma Y. Thyroid hormone and estrogen regulate brain region-specific messenger ribonucleic acids encoding three gonadotropin-releasing hormone genes in sexually immature male fish. Oreochromis niloticus, Endocrinol. 2000, 141:1618-1626.
54. Paris M., Hillenweck A., Bertrand S., Delous G., Escriva H., Zalko D., Cravedi J.P., Laudet V. Active metabolism of thyroid hormone during metamorphosis of amphioxus. Integr. Comp. Biol. 2010, 50:63-74.
55. Philp A.R., Garcia-Fernandez J.M., Soni B.G., Lucas R.J., Bellingham J., Foster R.G. Vertebrate ancient (VA) opsin and extraretinal photoreception in the Atlantic salmon (Salmo salar). J. Exp. Biol. 2000, 203:1925-1936.
56. Postlethwait J.H., Amores A., Cresko W.A., Singer A., Yan Y.L. Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet. 2004, 20:481-490.
57. Raine J.C. Hormones and reproduction of vertebrates. Hormones and reproduction of vertebrates 2010, 83-102. Elsevier Press, New York. D.O. Norris, K.H. Lopez (Eds.).
58. P.J. Sharp, Photoperiodic regulation of seasonal breeding in birds, Ann. N.Y. Acad. Sci. 1040 (2005) 189-199.
59. R Development Core Team R: A Language and Environment for Statistical Computing 2007, R Foundation for Statistical Computing, Vienna.
60. Thisse C., Thisse B., Schilling T.F., Postlethwait J.H. Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 1993, 119:1203-1215.
61. Yang Z. Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol. Evol. 1996, 11:367-372.
62. Yasuo S., Yoshimura T. Comparative analysis of the molecular basis of photoperiodic signal transduction in vertebrates. Integr. Comp. Biol. 2009, 49:507-518.
63. Yasuo S., Yoshimura T., Ebihara S., Korf H.W. Photoperiodic control of TSH-β expression in the mammalian pars tuberalis has different impacts on the induction and suppression of the hypothalamo-hypopysial gonadal axis. J. Neuroendocrinol. 2010, 22:43-50.
64. Yeates-Burghart Q.S., O'Brien C., Cresko W.A., Holzapfel C.M., Bradshaw W.E. Latitudinal variation in photoperiodic response of the three-spined stickleback Gasterosteus aculeatus in western North America. J. Fish Biol. 2009, 75:2075-2081.
65. Yoshimura T. Neuroendocrine mechanism of seasonal reproduction in birds and mammals. Animal Sci. J. 2010, 81:403-410.
66. Yoshimura T., Yasuo S., Watanabe M., Iigo M., Yamamura T., Hirunagi K., Ebihara S. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 2003, 426:178-181.
67. Zar J.H. Biostatistical Analysis 1996, Prentice Hall, Upper Saddle River, NJ, pp. 220-222.