Seasonal Changes in Hypothalamic Gonadotropin-Releasing Hormone-I Immunoreactivity in Relation With Testicular Volume in Adult Male Free-Living European Starlings (Sturnus Vulgaris)

Abstract

Birds from the temperate and cold zones show annual sexual activity accompanied by gonadal changes and fuctuation in their brain gonadotropin-releasing hormone (GnRH) levels. However, most of the studies were done on captive birds where the constant environment can profoundly modify periodical changes. Therefore our aim was to reveal annual variations of hypothalamic and gonadal changes in male, free-living European starlings (Sturnus vulgaris) captured directly from their natural environment. We analyzed hypothalamic GnRH-I immunoreactivity and testes volume. Four key time points of the active reproductive cycle and the photorefractory phase were studied. GnRH-I immunoreactivity was analyzed in the preoptic area (POA) and the median eminence (ME). Photorefractory birds (August) with regressed gonads had the lowest level of GnRH-I immunoreactivity compared to other birds from the active reproductive phases. These results suggest that parallel with the gonadal volume GnRH-I undergoes seasonal changes in adult male free-living European starlings.

Abbreviations

ABC:

avidin-biotin complex

FSH:

follicle-stimulating hormone

GnRH:

gonadotropin-releasing hormone

GnRH-ir:

GnRH immunoreactivity

KPBS:

potassium-phosphate buffer

L:D:

light/dark hours per day

LH:

luteinizing hormone

ME:

median eminence

POA:

preoptic area

TrSM:

tractus septomesenchephalicus

References

  1. 1.

    Bentley, G. E., Moore, I. T., Sower, S. A., Wingfield J. C. (2004) Evidence for a novel gonadotropin-releasing hormone in hypothalamic and forebrain areas in songbirds. Brain Behav. Evol. 63, 34–46.

    Article  Google Scholar 

  2. 2.

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

    CAS  Article  Google Scholar 

  3. 3.

    Dawson, A. (2004) Evidence against a period of relative photorefractoriness during the recovery of photosensitivity in common starlings. Gen. Comp. Endocrinol. 136, 117–121.

    CAS  Article  Google Scholar 

  4. 4.

    Dawson, A., Follett, B. K., Goldsmith, A. R., Nicholls T. J. (1987) Hypothalamic gonadotrophin-re-leasing hormone and pituitary and plasma FSH and prolactin during photostimulation and photorefractoriness in intact and thyroidectomized starlings (Sturnus vulgaris). J. Endocrinol. 115, 211–220.

    Article  Google Scholar 

  5. 5.

    Dawson, A., Goldsmith A. R. (1983) Plasma prolactin and gonadotrophins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J. Endocrinol. 97, 253–260.

    CAS  Article  Google Scholar 

  6. 6.

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

    CAS  Article  Google Scholar 

  7. 7.

    Dittami, J., Gwinner, E., Follett, B. K., Prossinger, H. (2005) Changes in circadian LH-secretion patterns and annual gonadal cycles in the male European starling (Sturnus vulgaris). J. Ornithol. 146, 338–347.

    Article  Google Scholar 

  8. 8.

    Follett, B. K., Maung S. L. (1978) Rate of testicular maturation, in relation to gonadotrophin and testosterone levels, in quail exposed to various artificial photoperiods and to natural day lengths. J. Endocrinol. 78, 267–280.

    CAS  Article  Google Scholar 

  9. 9.

    Foster, R. G., Panzica, G. C., Parry, D. M., Viglietti-Panzica, C. (1988) Immunocytochemical studies on the LHRH system of the Japanese quail: inluence by photoperiod and aspects of sexual differentiation. Cell Tissue Res. 253, 327–335.

    CAS  Article  Google Scholar 

  10. 10.

    Foster, R. G., Plowman, G., Goldsmith, A. R., Follett B. K. (1987) Immunohistochemical demonstration of marked changes in the LHRH system of photosensitive and photorefractory European starlings (Sturnus vulgaris). J. Endocrinol. 115, 211–220.

    CAS  Article  Google Scholar 

  11. 11.

    Hahn, T. P., Ball G. F. (1995) Changes in brain GnRH associated with photorefractoriness in house sparows (Passer domesticus). Gen. Comp. Endocrinol. 99, 349–363.

    CAS  Article  Google Scholar 

  12. 12.

    Kern, M. D. (1979) Seasonal changes in the reproductive system of the female white-crowned sparrow, Zonotrichia leucophrys gambelii, in captivity and in the field. 2. The incubation patch. Cell Tissue Res. 202, 379–398.

    CAS  Article  Google Scholar 

  13. 13.

    Kordonowy, L. L., McMurtry, J. P., Williams T. D. (2009) Variation in plasma leptin-like immunore-activity in free-living European starlings (Sturnus vulgaris). Gen. Comp. Endocrinol. 166, 47–53.

    Article  Google Scholar 

  14. 14.

    Lambrechts, M. M., Perret, P. (2000) Along photoperiod overrides non-photoperiodic factors in blue tits’ timing of reproduction. Proc. Biol. Sci. 267, 585–588.

    CAS  Article  Google Scholar 

  15. 15.

    Lambrechts, M. M., Perret, P., Maistre, M., Blondel, J. (1999) Do experiments with captive non-domesticated animals make sense without population field studies? A case study with blue tits’ breeding time. Proc. R. Soc. Lond. B 266, 1311–1315.

    Article  Google Scholar 

  16. 16.

    Maney, D. L., Richardson, R. D., Wingfield J. C. (1997) Central administration of chicken gonado-tropin-releasing hormone-II enhances courtship behavior in a female sparrow. Horm. Behav. 32, 11–18.

    CAS  Article  Google Scholar 

  17. 17.

    Meddle, S. L., Maney, D. L., Wingfield J. C. (1999) Effects of N-methyl-D-aspartate on luteinizing hormone release and Fos-like immunoreactivity in the male White-crowned sparrow (Zonotrichia leucophrys gambelii). Endocrinol. 140, 5922–5928.

    CAS  Article  Google Scholar 

  18. 18.

    Millam, J. R., Ottinger, M. A., Craig-Veit, C. B., Fan, Y., Chaiseha, Y., el Halawani, M. (1998) Multiple forms of GnRH are released from perifused medial basal hypothalamic/preoptic area (MBH/ POA) expiants in birds. Gen. Comp. Endocrinol. 111, 95–101.

    CAS  Article  Google Scholar 

  19. 19.

    Molnár, Gy. (1982) Populációökológiai vizsgálatok a Sturnus vulgarison. Doktori értekezés. JATE Állattani Tanszék, Szeged (in Hungarian).

    Google Scholar 

  20. 20.

    Nicholls, T. J., Goldsmith, A. R., Dawson, A. (1988) Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68, 133–176.

    CAS  Article  Google Scholar 

  21. 21.

    Parry, D. M., Goldsmith, A. R., Millar, R. P., Glennie L. M. (1997) Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness. J. Neuroendocrinal. 9, 235–243.

    CAS  Article  Google Scholar 

  22. 22.

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

    Article  Google Scholar 

  23. 23.

    Perfito, N., Bentley, G. E., Hau, M. (2006) Tonic activation of brain GnRH immunoreactivity despite reduction of peripheral reproductive parameters in opportunistically breeding zebra finches. Brain Behav. Evol. 67, 123–134.

    Article  Google Scholar 

  24. 24.

    Phillmore, L. S., Hoshooley, J. S., Hahn, T. P., MacDougall-Shackleton, S.A. (2005) Atest of absolute photorefractoriness and photo-induced neural plasticity of song-control regions in black-capped chickadees (Poecile atricapillus). Can. J. Zool. 83, 747–753.

    Article  Google Scholar 

  25. 25.

    Riters, L. V., Eens, M., Pinxten, R., Duffy, D. L., Balthazart, J., Ball G. F. (2000) Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm. Behav. 38, 250–261.

    CAS  Article  Google Scholar 

  26. 26.

    Robinson, J. E., Follett B. K. (1982) Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. R. Soc. Lond. B. Biol. Sci. 215, 95–116.

    CAS  Article  Google Scholar 

  27. 27.

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

    CAS  Article  Google Scholar 

  28. 28.

    Small, W. T., Sharp, P. J., Bentley, G. E., Millar, R. P., Tsutsui, K., Mura, E., Deviche, P. (2008) Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living sonoran desert bird, the rufous-winged sparrow (Aimophila carpalis). Brain. Behav. Evol. 71, 127–142.

    Article  Google Scholar 

  29. 29.

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

    CAS  Article  Google Scholar 

  30. 30.

    Stevenson, T. J., Bernard, D. J., Ball G. F. (2009) Photoperiodic condition is associated with region-specific expression of GNRH1 mRNA in the preoptic area of the male starling (Sturnus vulgaris). Biol. Reprod. 81, 674–680.

    CAS  Article  Google Scholar 

  31. 31.

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

    CAS  Article  Google Scholar 

  32. 32.

    Stevenson, T. J., Macdougall-Shackleton, S. A. (2005) Season- and age-related variation in neural cGnRH-I and cGnRH-II immunoreactivity in house sparrows (Passer domesticus). Gen. Comp. Endocrinol. 143, 33–39.

    CAS  Article  Google Scholar 

  33. 33.

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

    CAS  Article  Google Scholar 

  34. 34.

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

    CAS  Article  Google Scholar 

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Correspondence to O. Pintér.

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Pintér, O., Péczel, P. Seasonal Changes in Hypothalamic Gonadotropin-Releasing Hormone-I Immunoreactivity in Relation With Testicular Volume in Adult Male Free-Living European Starlings (Sturnus Vulgaris). BIOLOGIA FUTURA 61, 237–249 (2010). https://doi.org/10.1556/ABiol.61.2010.3.1

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Keywords

  • European starling
  • seasonal reproduction
  • GnRH-I
  • testes
  • immunohistochemistry