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Photoperiodic control of GnRH-I expression in seasonal reproduction of the Eurasian tree sparrow

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Abstract

Day length has been shown to be a major source of temporal information regulating seasonal reproduction in the Eurasian tree sparrow (Passer montanus). The present study aims to investigate the photoperiodic expression of gonadotropin-releasing hormone-I (GnRH-I), and how it mediates seasonal reproduction in male tree sparrows. In different experiments, we studied photoperiod-induced changes in GnRH-I expressing neurons in the hypothalamic preoptic area (POA), together with changes in testicular size under both natural and artificial photoperiodic conditions. Experiment 1, which involved studying changes in GnRH-I expression and testicular volume during different phases of the annual reproductive cycle under natural day length (NDL), revealed that sparrows possess a definite seasonal cycle of GnRH-I peptide expression that runs parallel to testicular size. Birds showed significantly higher levels of GnRH-I expression in the breeding phase when compared to the non-breeding phase. In experiment 2, photosensitive birds were exposed to artificial short (SD: 9L/15D) and long (LD: 14L/10D) day lengths for 240 days to investigate the photoperiodic regulation of GnRH-I expression. They exhibited a significant increase followed by a decrease in GnRH-I expression and testicular size under LD but not SD, suggesting photoperiodic regulation. In experiment 3, when photosensitive birds were exposed to increasing photo-periods (9L/15D, 10L/14D, 10.5L/13.5D, 11L/13D, 12L/12D) for 30 days to find out the critical photoperiod for GnRH-I expression, they responded only when the daily photoperiod was 11 h or more. These results clearly indicate that tree sparrows are capable of fine discrimination of photoperiodic information and use day length for GnRH-I expression to control their seasonal reproduction.

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References

  1. A. S. Dixit and N. S. Singh, Photoperiod as a proximate factor in control of seasonality in the subtropical male tree sparrow, Passer montanus, Front. Zool., 2011, 8, 1.

    PubMed  PubMed Central  Google Scholar 

  2. B. D. Goldman, Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement, J. Biol. Rhythms, 2001, 16, 283–301.

    Article  CAS  PubMed  Google Scholar 

  3. A. Dawson, V. M. King, G. E. Bentley and G. F. Ball, Photoperiodic control of seasonality in birds, J. Biol. Rhythms, 2001, 16, 366–381.

    Article  Google Scholar 

  4. T. J. Stevenson and G. F. Ball, Anatomical localization of the effects of reproductive state, castration, and social milieu on cells immunoreactive for gonadotropin-releasing hormone 1 in male European starlings, J. Comp. Neurol., 2009, 517, 146–155.

    Article  CAS  PubMed  Google Scholar 

  5. A. S. Dixit, N. S. Singh and S. Byrsat, Role of GnIH in photoperiodic regulation of seasonal reproduction in the Eurasian tree sparrow, J. Exp. Biol., 2007, 220, 3742–3750.

    Article  Google Scholar 

  6. M. Hau, M. Wikelski, H. Gwinner and E. Gwinner, Timing of reproduction in a Darwin's finch: temporal opportunism under spatial constraints, Oikos, 2004, 489, 489–500.

    Article  Google Scholar 

  7. W. E. Bradshaw and C. M. Holzapfel, Genetic response to rapid climate change: it's seasonal timing that matters, Mol. Ecol., 2007, 17, 157–166.

    Article  PubMed  Google Scholar 

  8. A. S. Dixit, N. S. Singh and R. Sougrakpam, A comparative study on photoperiodic control of seasonal cycle in the females of migratory breasted bunting and the resident tree sparrow, Photochem. Photobiol. Sci., 2014, 13, 1568–1579.

    Article  CAS  PubMed  Google Scholar 

  9. J. C. Wingfield and G. J. Kenagy, Natural regulation of reproductive cycles, in Vertebrate Endocrinology: Fundamentals and Biomedical Implications, ed. M. Schreibman and R. E. Jones, Academic Press, New York, 1991, pp. 181–241.

    Google Scholar 

  10. Surbhi, A. Rastogi, S. Rani and V. Kumar, Seasonal plasticity in the peptide neuronal systems: potential roles of gonadotrophin-releasing hormone, gonadotrophin inhibiting hormone, neuropeptide Y and vasoactive intestinal peptide in the regulation of the reproductive axis in subtropical Indian weaver birds, J. Neuroendocrinol., 2015, 27, 357–369.

    Article  CAS  PubMed  Google Scholar 

  11. P. J. Sharp, R. T. Talbot, G. M. Main, I. C. Dunn, H. M. Fraser and N. S. Huskisson, Physiological roles of chicken LHRH-I and -II in the control of gonadotrophin release in the domestic chicken, J. Endocrinol., 1990, 124, 291–299.

    Article  CAS  PubMed  Google Scholar 

  12. D. L. Maney, R. D. Richardson and J. C. Wingfield, Central administration of chicken gonadotropin II enhances courtship behaviour in a female sparrow, Horm. Behav., 1997, 32, 11–18.

    Article  CAS  PubMed  Google Scholar 

  13. R. P. Millar, GnRH II and type II GnRH receptors, Trends Endocrinol. Metab., 2003, 14, 35–43.

    Article  CAS  PubMed  Google Scholar 

  14. T. S. Juss, G. F. Ball and D. M. Parry, Immunocytochemical localization of cGnRH-I and cGnRH-II in the brains of photosensitive and photorefractory European starlings and Japanese quail, Proceedings of the Fifth International Symposium on Avian Endocrinology, Edinburgh, Scotland, 1992, p 87.

    Google Scholar 

  15. J. R. Millam, P. L. Faris, O. M. Youngren, M. E. El Halawani and B. K. Hartman, Immunohistochemical localization of chicken gonadotropin-releasing hormones I and II (cGnRH I and II) in Turkey Hen Brain, J. Comp. Neurol., 1993, 333, 68–82.

    Article  CAS  PubMed  Google Scholar 

  16. T. J. Stevenson, T. P. Hahn and G. F. Ball, Variation in gonadotropin releasing-hormone-1 gene expression in the preoptic area predicts transitions in seasonal reproductive state, J. Neuroendocrinol., 2012, 24, 267–274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. A. Dawson, B. K. Follett, A. R. Goldsmith and T. J. Nicholls, Hypothalamic gonadotrophin-releasing hormone and pituitary and plasma FSH and prolactin during photostimulation and photorefractoriness in intact and thyroidectomized starlings (Sturnus vulgaris), J. Endocrinol., 1985, 105, 71–77.

    Article  CAS  PubMed  Google Scholar 

  18. G. F. Ball and T. P. Hahn, GnRH neuronal systems in birds and their relation to the control of seasonal reproduction, in GnRH Neurons: Gene to Behavior, ed. I. S. Parhar and Y. Sakuma, Brain Shuppan Publishers, Tokyo, 1997, pp. 325–342.

    Google Scholar 

  19. N. Perfito, R. Zann, T. Ubuka, G. E. Bentley and M. Hau, Potential roles for GnIH and GnRH-II in reproductive axis regulation of an opportunistically breeding songbird, Gen. Comp. Endocrinol., 2011, 173, 20–26.

    Article  CAS  PubMed  Google Scholar 

  20. A. Dawson, Annual gonadal cycles in birds: modelling the effects of photoperiod on seasonal changes in GnRH secretion, Front. Neuroendocrinol., 2015, 37, 52–64.

    Article  CAS  PubMed  Google Scholar 

  21. Surbhi and V. Kumar, Avian photoreceptors and their role in the regulation of daily and seasonal physiology, Gen. Comp. Endocrinol., 2015, 220.

    Google Scholar 

  22. H. Li and W. J. Keunzel, A possible neural cascade involving the photoneuroendocrine system (PNES) responsible for regulating gonadal development in an avian species, Gallus gallus, Brain Res. Bull., 2008, 76, 586–596.

    Article  CAS  PubMed  Google Scholar 

  23. W. I. L. Davies, M. Turton, S. N. Pierson, B. K. Follet, S. Halford, J. M. Garcia-Fernandes, P. J. Sharp, M. W. Hankins and R. G. Foster, Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response, Biol. Lett., 2012, 8, 291–294.

    Article  PubMed  Google Scholar 

  24. Y. Nakane, T. Shimmura, H. Abe and T. Yoshimura, Intrinsic photosensitivity of a deep brain photoreceptor, Curr. Biol., 2014, 24, 596–597.

    Article  CAS  Google Scholar 

  25. C. J. Saldanha, A. J. Silverman and R. Silver, Direct innervations of GnRH neurons by encephalic photoreceptors, J. Biol. Rhythms, 2001, 16, 39–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. T. Yoshimura, Neuroendocrine mechanism of seasonal reproduction in birds and mammals, Anim. Sci. J., 2010, 81, 403–410.

    Article  CAS  PubMed  Google Scholar 

  27. W. J. Kuenzel, S. W. Kang and Z. J. Zhou, Exploring avian deep brain photoreceptors and their role in activating the neuroendocrine regulation of gonadal development, Poult. Sci., 2015, 94, 786–798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Y. Nakane, K. Ikegami, H. Ono, N. Yamamoto and S. Yoshida, 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. N. Nakao, H. Ono, T. Yamamura, T. Anraku, T. Takagi and K. Higashi, Thyrotrophin in the pars tuberalis triggers photoperiodic response, Nature, 2008, 452, 317–322.

    Article  CAS  PubMed  Google Scholar 

  30. T. J. Stevenson and G. F. Ball, Disruption of neuropsin mRNA expression via RNA interference facilitates the photoinduced increase in thyrotropin-stimulating subunit ss in birds, Eur. J. Neurosci., 2012, 36, 2859–2865.

    Article  PubMed  Google Scholar 

  31. T. Yoshimura, S. Yasuo, M. Watanabe, M. Iigo, T. Yamamura and K. Hirunagi, Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds, Nature, 2003, 426, 178–181.

    Article  CAS  PubMed  Google Scholar 

  32. S. Yasuo, M. Watanabe, N. Nakao, T. Takagi, B. K. Follett, S. Ebihara and T. Yoshimura, The reciprocal switching of two thyroid hormone-activating and - inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail, Endocrinol., 2005, 146, 2551–2554.

    Article  CAS  Google Scholar 

  33. T. Watanabe, T. Yamamura, M. Watanabe, S. Yasuo, N. Nakao, A. Dawson, S. Ebihara and T. Yoshimura, Hypothalamic expression of thyroid hormone activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2007, 292, 568–572.

    Google Scholar 

  34. T. Yamamura, K. Hirunagi, S. Ebihara and T. Yoshimura, Seasonal morphological changes in the neuro-glial interaction between gonadotropin releasing hormone nerve terminals and glial end feet in Japanese quail, Endocrinol., 2004, 145, 4264–4267.

    Article  CAS  Google Scholar 

  35. T. Yamamura, S. Yasuo, K. Hirunagi, S. Ebihara and T. Yoshimura, T-3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail, Cell Tissue Res., 2006, 324, 175–179.

    Article  CAS  PubMed  Google Scholar 

  36. A. Srivastava, N. Trivedi, S. Malik, S. Rani and V. Kumar, Molecular basis of photoperiodic control of reproductive cycle in a subtropical songbird, the Indian weaver bird (Ploceus philippinus), Gen. Comp. Endocrinol., 2015, 220, 41–45.

    Article  CAS  PubMed  Google Scholar 

  37. K. Tsutsui, E. Saigoh, K. Ukena, H. Teranishi, Y. Fujisawa, M. Kikuchi, S. Ishii and P. J. Sharp, A novel avian hypothalamic peptide inhibiting gonadotropin release, Biochem. Biophys. Res. Commun., 2001, 275, 661–667.

    Article  CAS  Google Scholar 

  38. K. Tsutsui, T. Ubuka, G. E. Bentley and L. J. Kriegsfeld, Regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals, Front. Neurosci., 2013, 7, 60.

    Article  PubMed  PubMed Central  Google Scholar 

  39. A. S. Dixit and N. S. Singh, Seasonal variation in sensitivity of the photoperiodic response system in the subtropical tree sparrow (Passer montanus), J. Exp. Zool., 2012, 999, 1–11.

    Google Scholar 

  40. A. S. Dixit and N. S. Singh, Participation of endogenous circadian rhythm in photoperiodic time measurement during ovarian responses of the sub tropical tree sparrow, Passer montanus, Indian J. Exp. Biol., 2013, 52, 496–503.

    Google Scholar 

  41. A. Rastogi, Y. Kumari, S. Rani and V. Kumar, Phase inversion of neural activity in the olfactory and visual systems of a night-migratory bird during migration, Eur. J. Neurosci., 2011, 34, 99–109.

    Article  PubMed  Google Scholar 

  42. H. F. Urbanski, S. O. Kim and M. L. Connolly, Influence of photo period and 6-methoxy benzoxazolinone on the reproductive axis of inbred LSH/Ss Lak male hamsters, J. Reprod. Fertil., 1990, 26, 437–444.

    Google Scholar 

  43. H. F. Urbanski, Photoperiod and modulation of luteinizing hormone secretion in orchidectomized Syrian hamsters and the influence of excitatory amino acids, Endocrinol., 1992, 131, 1665–1669.

    Article  CAS  Google Scholar 

  44. T. Ubuka and G. E. Bentley, Identification, localization, and regulation of passerine GnRH-I messenger RNA, J. Endocrinol., 2009, 201, 81–87.

    Article  CAS  PubMed  Google Scholar 

  45. T. Ubuka, S. Kim, Y. C. Huang, J. Reid, J. Jiang, T. Osugi, V. S. Chowdhury, K. Tsutsui and G. E. Bentley, Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and–II neurons in European starling brain, Endocrinol., 2008, 149, 268–278.

    Article  CAS  Google Scholar 

  46. A. Rastogi, Y. Kumari, S. Rani and V. Kumar, Neural correlates of migration: activation of hypothalamic clock (s) in and out of migratory state in the blackheaded bunting (Emberiza melanocephala), PLoS One, 2013, 8, 10.

    Article  CAS  Google Scholar 

  47. T. P. Hahn and G. F. Ball, Changes in brain GnRH associated with photorefractoriness in house sparrows, Gen. Comp. Endocrinol., 1995, 99, 349–363.

    Article  CAS  PubMed  Google Scholar 

  48. Surbhi, A. Rastogi, S. Malik, S. Rani and V. Kumar, Changes in brain peptides associated with reproduction and energy homeostasis in photosensitive and photorefractory migratory redheaded buntings, Gen. Comp. Endocrinol., 2016, 230–231, 67–75.

    Article  PubMed  CAS  Google Scholar 

  49. R. G. Foster, G. Plowman, A. R. Goldsmith and B. K. Follett, Immunocytochemical demonstration of marked changes in the luteinizing hormone-releasing hormone system of photosensitive and photorefractory European starlings, J. Endocrinol., 1987, 115, 211–220.

    Article  CAS  PubMed  Google Scholar 

  50. J. C. Wingfield and D. S. Farner, Endocrinology of reproduction in wild species, Avian Biol., 1993, 9, 163–327.

    Google Scholar 

  51. B. D. Reinert and F. E. Wilson, The thyroid and the hypothalamus-pituitary ovarian-axis in American tree sparrows (Spizella arborea), Gen. Comp. Endocrinol., 1996, 103, 60–70.

    Article  CAS  PubMed  Google Scholar 

  52. R. N. Cho, T. P. Hahn, S. A. MacDougall-Shackleton and G. F. Ball, Seasonal variation in brain GnRH in free-living breeding and photorefractory House finches (Carpodacus mexicanus), Gen. Comp. Endocrinol., 1998, 109, 244–250.

    Article  CAS  PubMed  Google Scholar 

  53. S. L. Meddle, S. Bush, P. J. Sharp, R. P. Millar and J. C. Wingfield, Hypothalamic pro- GnRH GnRH-II during the onset of photorefractoriness in the white-crowned sparrow (Zonotrichia leucophrys gambelii), J. Neuroendocrinol., 2006, 18, 217–226.

    Article  CAS  PubMed  Google Scholar 

  54. A. Dawson and A. R. Goldsmith, Changes in gonadotropin-releasing hormone (GnRH-I) in the preoptic area and median eminence of starlings (Sturnus vulgaris) during the recovery of photosensitivity and during photostimulation, J. Reprod. Fertil., 1997, 111, 1–6.

    Article  CAS  PubMed  Google Scholar 

  55. S. A. MacDougall-Shackleton, T. J. Stevenson, H. E. Watts, M. E. Pereyra and T. P. Hahn, The evolution of photoperiod response systems and seasonal GnRH plasticity in birds, Integr. Comp. Biol., 2009, 49, 580–589.

    Article  CAS  PubMed  Google Scholar 

  56. M. E. Pereyra, S. M. Sharbaug and T. P. Hahn, Interspecific variation in photo-induced GnRH plasticity among nomadic cardueline finches, Brain, Behav. Evol., 2005, 66, 35–49.

    Article  Google Scholar 

  57. E. L. Sansum and J. R. King, Long term effects of constant photoperiods on testicular cycles of white crowned sparrow, Zonotrichia leucophrys gambelii, Physiol. Zool., 1976, 49, 407–416.

    Article  Google Scholar 

  58. T. W. Small, P. J. Sharp, G. E. Bentley and P. Deviche, Relative photorefractoriness, prolactin, and reproductive regression in a flexibly breeding Sonoran Desert passerine, the rufous-winged sparrow, Aimophila carpalis, J. Biol. Rhythms, 2008, 23, 69–80.

    Article  CAS  PubMed  Google Scholar 

  59. T. Ubuka, P. A. Cadigan, A. Wang, J. Liu and G. E. Bentley, Identification of European starling GnRH-I precursor mRNA and its seasonal regulation, Gen. Comp. Endocrinol., 2009, 162, 301–306.

    Article  CAS  PubMed  Google Scholar 

  60. T. J. Stevenson, K. S. Lynch, P. Lamba, G. F. Ball and D. J. Bernard, Cloning of gonadotropin- releasing hormone I complementary DNAs in songbirds facilitates dissection of mechanisms mediating seasonal changes in reproduction, Endocrinol., 2009, 150, 1826–1833.

    Article  CAS  Google Scholar 

  61. T. D. Siopes and W. O. Wilson, Extraocular modification of photoreception in intact and pinealectomized Coturnix, Poult. Sci., 1974, 53, 2035–2041.

    Article  CAS  PubMed  Google Scholar 

  62. J. Benoit, Rrle de loeil dans la gonadostimulation par la lumi∼rechez les Oiseaux, Ann. Biol., 1974, 13, 187–195.

    Google Scholar 

  63. S. Banerjee, Neuroendocrine mechanism of reproduction and energy regulation in Japanese quail, Coturnix coturnix japonica, Ph. D. thesis, Banaras Hindu University, Varanasi, India, 2016.

    Google Scholar 

  64. G. E. Bentley, N. Perfito, K. Ukena, K. Tsutsui and J. C. Wingfield, Gonadotropin-inhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone, J. Neuroendocrinol., 2003, 15, 794–802.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Financial supports from the Department of Biotechnology and Department of Science and Technology, Government of India, New Delhi are gratefully acknowledged. We are also grateful to Professor Henryk F. Urbanski (Oregon Health and Sciences University, Portland, Oregon, USA) for kindly providing the rabbit anti-GnRH antibody.

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Correspondence to Anand S. Dixit.

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Dixit, A.S., Byrsat, S. Photoperiodic control of GnRH-I expression in seasonal reproduction of the Eurasian tree sparrow. Photochem Photobiol Sci 17, 934–945 (2018). https://doi.org/10.1039/c8pp00153g

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