Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Limin Wang, Ghulam Nabi, Li Zhang, Dan Liu, Mo Li, Juyong Li, Kaixin Shi, Ibrahim M. Ahmad, Yuefeng Wu, John C. Wingfield, Dongming Li. 2022: Seasonal variations in gonad morphology and hypothalamic GnRH-I and GnIH in Eurasian Tree Sparrow, a multi-brooded passerine. Avian Research, 13(1): 100037. doi: 10.1016/j.avrs.2022.100037
Citation: Limin Wang, Ghulam Nabi, Li Zhang, Dan Liu, Mo Li, Juyong Li, Kaixin Shi, Ibrahim M. Ahmad, Yuefeng Wu, John C. Wingfield, Dongming Li. 2022: Seasonal variations in gonad morphology and hypothalamic GnRH-I and GnIH in Eurasian Tree Sparrow, a multi-brooded passerine. Avian Research, 13(1): 100037. doi: 10.1016/j.avrs.2022.100037

Seasonal variations in gonad morphology and hypothalamic GnRH-I and GnIH in Eurasian Tree Sparrow, a multi-brooded passerine

doi: 10.1016/j.avrs.2022.100037
More Information
  • Corresponding author: E-mail address: lidongming@hebtu.edu.cn (D. Li)
  • Received Date: 18 Mar 2022
  • Accepted Date: 08 May 2022
  • Rev Recd Date: 05 May 2022
  • Available Online: 11 Oct 2022
  • Publish Date: 18 May 2022
  • The hypothalamic-pituitary-gonadal (HPG) axis ubiquitously regulates seasonal reproduction, following the rhythmicity of a suite of environmental cues. Birds display prominent seasonal variations in gonad size regulated by two hypothalamic peptides, gonadotropin-releasing hormone-1 (GnRH-I) and gonadotropin-inhibiting hormone (GnIH). How multi-brooded avian species adjust GnRH-I and GnIH to regulate gonadal morphology seasonally remains largely unknown. Here, we studied the variations in the hypothalamic immunoreactivity (ir) of GnRH-I and GnIH, gonadal proliferation, and apoptosis in a typical multi-brooded species, the Eurasian Tree Sparrow (Passer montanus), across the pre-breeding (PB), first breeding (FB), second breeding (SB), pre-basic molt (PM), and wintering stages (WS). Our results showed that both sexes had higher preoptic area (POA)-GnRH-I-ir but lower paraventricular nucleus (PVN)-GnIH-ir neurons during the breeding stages (FB and SB) relative to other life-history stages, with no significant differences between two broods. The testes and ovaries were significantly larger during the breeding stages. Testicular volume increased during the two broods due to anincreased diameter of seminiferous tubules. Furthermore, there were more testicular apoptotic cells in PB and WS stages than in breeding stages, and in PB stage than in PM stage. Males had higher POA-GnRH-I expression than females during the breeding stages, but both sexes had comparable PVN-GnIH expression throughout the annual cycle. Both sexes of the sparrows may undergo a similar pattern of life-history stage-dependent variation in the hypothalamic GnRH-I, GnIH, and gonadal morphology, except that during breeding stages, males may display higher expression of POA-GnRH-I relative to females. The higher expression of POA-GnRH-I-ir in breeding male sparrows may be critical for male-dependent parental care.


  • 1 These two authors contributed equally to this work.
  • loading
  • Akhtar, M.F., Ahmad, E., Mustafa, S., Chen, Z., Shi, Z., Shi, F., 2020. Spermiogenesis, stages of seminiferous epithelium and variations in seminiferous tubules during active states of spermatogenesis in Yangzhou goose ganders. Animals (Basel). 10, 1-13. https://doi.org/10.3390/ani10040570.
    Amorin, N., Calisi, R.M., 2015. Measurements of neuronal soma size and estimated peptide concentrations in addition to cell abundance offer a higher resolution of seasonal and reproductive influences of GnRH-I and GnIH in European starlings. Integr. Comp. Biol. 55, 332-342. https://doi.org/10.1093/icb/icv063.
    Ball, G.F., Ketterson, E.D., 2008. Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos. Trans. R Soc. Lond. B Biol. Sci. 363, 231-246. https://doi.org/10.1098/rstb.2007.2137.
    Banerjee, S., Chaturvedi, C.M., 2017. Testicular atrophy and reproductive quiescence in photorefractory and scotosensitive quail: involvement of hypothalamic deep brain photoreceptors and GnRH-GnIH system. J. Photochem. Photobiol. B. 175, 254-268. https://doi.org/10.1016/j.jphotobiol.2017.09.005.
    Banerjee, S., Tsutsui, K., Chaturvedi, C.M., 2016. Apoptosis-mediated testicular alteration in Japanese quail (Coturnix coturnix japonica) in response to temporal phase relation of serotonergic and dopaminergic oscillations. J. Exp. Biol. 219, 1476-1487. https://doi.org/10.1242/jeb.129155.
    Bauer, C.M., Fudickar, A.M., Anderson-Buckingham, S., Abolins-Abols, M., Atwell, J.W., Ketterson, E.D., et al., 2018. Seasonally sympatric but allochronic: differential expression of hypothalamic genes in a songbird during gonadal development. Proc. Biol. Sci. 285, 20181735. https://doi.org/10.1098/rspb.2018.1735.
    Bentley, G.E., Ubuka, T., McGuire, N.L., Chowdhury, V.S., Morita, Y., Yano, T., et al., 2008. Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen. Comp. Endocrinol. 156, 34-43. https://doi.org/10.1016/j.ygcen.2007.10.003.
    Bhavna, B., Geeta, P., 2010. Histological and histomorphometric study of gametogenesis in breeders and helpers of sub-tropical, co-operative breeder jungle babbler, Turdoides striatus. J. Cell Anim. Biol. 4, 81-90. https://doi.org/10.5897/JCAB.9000090.
    Buttemer, W.A., Addison, B.A., Klasing, K.C., 2020. The energy cost of feather replacement is not intrinsically inefficient. Can. J. Zool. 98, 142-148. https://doi.org/10.1139/cjz-2019-0170.
    Cui, Y.M., Wang, J., Zhang, H.J., Qi, G.H., Wu, S.G., 2021. Effects of photoperiod on performance, ovarian morphology, reproductive hormone level, and hormone receptor mRNA expression in laying ducks. Poult. Sci. 100, 100979. https://doi.org/10.1016/j.psj.2021.01.002.
    Dawson, A., 2003. A comparison of the annual cycles in testicular size and moult in captive European starlings Sturnus vulgaris during their first and second years. J. Avian Biol. 34, 119-123. https://doi.org/10.2307/3677650.
    Dawson, A., 2007. Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods. Proc. Biol. Sci. 274, 721-725. https://doi.org/10.1098/rspb.2006.0067.
    Dawson, A., 2008. Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1621-1633. https://doi.org/10.1098/rstb.2007.0004.
    Dawson, A., Goldsmith, A.R., 1984. Effects of gonadectomy on seasonal changes in plasma LH and prolactin concentrations in male and female starlings (Sturnus vulgaris). J. Endocrinol. 100, 213-218. https://doi.org/10.1677/joe.0.1000213.
    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. https://doi.org/10.1530/jrf.0.1110001.
    Dawson, A., King, V.M., Bentley, G.E., Ball, G.F., 2001. Photoperiodic control of seasonality in birds. J. Biol. Rhythms. 16, 365-380. https://doi.org/10.1177/074873001129002079.
    Dawson, A., Talbot, R.T., Dunn, I.C., Sharp, P.J., 2002. Changes in basal hypothalamic chicken gonadotropin-releasing hormone-I and vasoactive intestinal polypeptide associated with a photo-induced cycle in gonadal maturation and prolactin secretion in intact and thyroidectomized starlings (Sturnus vulgaris). J. Neuroendocrinol. 14, 533-539. https://doi.org/10.1046/j.1365-2826.2002.00807.x.
    Deviche, P., Hurley, L.L., Fokidis, H.B., 2011. Avian testicular structure, function, and regulation. In: Norris, D.O., Lopez, H. (Eds. ), Hormones and Reproduction of Vertebrates: Birds. Academic Press, Pittsburgh, pp. 27–70.
    Ding, B.Y., Zhao, Y.L., Sun, Y.F., Zhang, Q., Li, M., Nabi, G., et al., 2021. Coping with extremes: lowered myocardial phosphofructokinase activities and glucose content but increased fatty acids content in highland Eurasian Tree Sparrows. Avian Res. 12, 44. https://doi.org/10.1186/s40657-021-00279-0.
    Dixit, A.S., Byrsat, S., 2018. Photoperiodic control of GnRH-I expression in seasonal reproduction of the Eurasian tree sparrow. Photochem. Photobiol. Sci. 17, 934-945. https://doi.org/10.1039/c8pp00153g.
    Dixit, A.S., Singh, N.S., 2013. Environmental control of seasonal reproduction in the wild and captive Eurasian tree sparrow (Passer montanus) with respect to variations in gonadal mass, histology, and sex steroids. Can. J. Zool. 91, 302-312. https://doi.org/10.1139/cjz-2012-0190.
    Dixit, A.S., Singh, N.S., 2014. Photoperiodic control of testicular growth, histomorphology and serum testosterone levels in the male Eurasian tree sparrow: involvement of circadian rhythm. Gen. Comp. Endocrinol. 208, 5-11. https://doi.org/10.1016/j.ygcen.2014.09.003.
    Dixon, A., Ward, J., Ichinkhorloo, S., Erdenechimeg, T., Galtbalt, B., Davaasuren, B., et al., 2021. Seasonal variation in gonad physiology indicates juvenile breeding in the Saker Falcon (Falco cherrug). Avian Biol. Res. 14, 39-47. https://doi.org/10.1177/1758155920971823.
    Falvo, S., Rosati, L., Di Fiore, M.M., Di Giacomo Russo, F., Chieffi Baccari, G.C., Santillo, A., 2021. Proliferative and apoptotic pathways in the testis of quail Coturnix coturnix during the seasonal reproductive cycle. Animals (Basel). 11, 1-15. https://doi.org/10.3390/ani11061729.
    Follett, B.K., 2015. Seasonal changes in the neuroendocrine system: some reflections. Front. Neuroendocrinol. 37, 3-12. https://doi.org/10.1016/j.yfrne.2014.11.003.
    George, E.M., Navarro, D., Rosvall, K.A., 2021. A single GnRH challenge promotes paternal care, changing nestling growth for one day. Horm. Behav. 130, 104964. https://doi.org/10.1016/j.yhbeh.2021.104964.
    Hahn, T.P., Ball, G.F., 1995. Changes in brain GnRH associated with photorefractoriness in house sparrows (Passer domesticus). Gen. Comp. Endocrinol. 99, 349-363. https://doi.org/10.1006/gcen.1995.1119.
    Halupka, L., Halupka, K., 2017. The effect of climate change on the duration of avian breeding seasons: a meta-analysis. Proc. Biol. Sci. 284, 20171710. https://doi.org/10.1098/rspb.2017.1710.
    Hanlon, C., Takeshima, K., Bédécarrats, G.Y., 2021. Changes in the control of the hypothalamic-pituitary gonadal axis across three differentially selected strains of laying hens (Gallus gallus domesticus). Front. Physiol. 12, 651491. https://doi.org/10.3389/fphys.2021.651491.
    Heninger, N.L., Staub, C., Blanchard, T.L., Johnson, L., Varner, D.D., Forrest, D.W., 2004. Germ cell apoptosis in the testes of normal stallions. Theriogenology. 62, 283-297. https://doi.org/10.1016/j.theriogenology.2003.10.022.
    Hurley, L.L., Wallace, A.M., Sartor, J.J., Ball, G.F., 2008. Photoperiodic induced changes in reproductive state of border canaries (Serinus canaria) are associated with marked variation in hypothalamic gonadotropin-releasing hormone immunoreactivity and the volume of song control regions. Gen. Comp. Endocrinol. 158, 10-19. https://doi.org/10.1016/j.ygcen.2008.05.011.
    Hurley, L.L., Crino, O.L., Rowe, M., Griffith, S.C., 2020. Variation in female reproductive tract morphology across the reproductive cycle in the zebra finch. Peer. J. 8, e10195. https://doi.org/10.7717/peerj.10195.
    Ioannidis, J., Taylor, G., Zhao, D., Liu, L., Idoko-Akoh, A., Gong, D., et al., 2021. Primary sex determination in birds depends on DMRT1 dosage, but gonadal sex does not determine adult secondary sex characteristics. Proc. Natl. Acad. Sci. USA. 118, e2020909118. https://doi.org/10.1073/pnas.2020909118.
    Jacobs, J.D., Wingfield, J.C., 2000. Endocrine control of life-cycle stages: a constraint on response to the environment? Condor. 102, 35-51. https://doi.org/10.2307/1370406.
    Jenkins, L.K., Ross, W.L., Young, K.A., 2007. Increases in apoptosis and declines in BcI-XL protein characterize testicular regression in American crows (Corvus brachyrhynchos). Reprod. Fertil. Dev. 19, 461-469. https://doi.org/10.1071/rd06079.
    Kriegsfeld, L.J., Ubuka, T., Bentley, G.E., Tsutsui, K., 2015. Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals. Front. Neuroendocrinol. 37, 65-75. https://doi.org/10.1016/j.yfrne.2014.12.001.
    Li, X., Su, J., Lei, Z., Zhao, Y., Jin, M., Fang, R., et al., 2012. Gonadotropin inhibitory hormone (GnIH) and its receptor in the female pig: cDNA cloning, expression in tissues and expression pattern in the reproductive axis during the estrous cycle. Peptides. 36, 176-185. https://doi.org/10.1016/j.peptides.2012.05.008.
    Li, D.M., Zhang, J., Liu, D., Zhang, L., Hu, Y.H., Duan, X.L., et al., 2013. Coping with extreme: highland Eurasian tree sparrows with molt-breeding overlap express higher levels of Corticoserone-binding globulin than lowland sparrows. J. Exp. Zool. A Ecol. Genet. Physiol. 319, 482-486. https://doi.org/10.1002/jez.1811.
    Li, D.M., Davis, J.E., Sun, Y.F., Wang, G., Nabi, G., Wingfield, J.C., et al., 2020a. Coping with extremes: convergences of habitat use, territoriality, and diet in summer but divergences in winter between two sympatric snow finches on the Qinghai-Tibet Plateau. Integr. Zool. 15, 533-543. https://doi.org/10.1111/1749-4877.12462.
    Li, D.M., Davis, J.E., Wang, G., Nabi, G., Bishop, V.R., Sun, Y.F., et al., 2020b. Coping with extremes: remarkably blunt adrenocortical responses to acute stress in two sympatric snow finches on the Qinghai-Tibet Plateau during winter relative to other seasons. Gen.Comp. Endocr. 291, 113434. https://doi.org/10.1016/j.ygcen.2020.113434.
    Li, L., Ge, J.R., Zheng, S.Y., Hong, L.H., Zhang, X.N., Li, M., et al., 2020. Thermogenic responses in Eurasian Tree Sparrow (Passer montanus) to seasonal acclimatization and temperature-photoperiod acclimation. Avian Res. 11, 35. https://doi.org/10.1186/s40657-020-00222-9.
    Li, M., Zhu, W.W., Wang, Y., Sun, Y.F., Li, J.Y., Liu, X.L., et al., 2019. Effects of capture and captivity on plasma corticosterone and metabolite levels in breeding Eurasian Tree Sparrows. Avian Res. 10, 16. https://doi.org/10.1186/s40657-019-0155-8.
    Li, Y.Q., Sun, Y.F., Krause, J.S., Li, M., Liu, X.L., Zhu, W.W., et al., 2017. Dynamic interactions between corticosterone, corticosteroid binding globulin and testosterone in response to capture stress in male breeding Eurasian tree sparrows. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 205, 41-47. https://doi.org/10.1016/j.cbpa.2016.12.016.
    MacDougall-Shackleton, S.A., Stevenson, T.J., Watts, H.E., Pereyra, M.E., Hahn, T.P., 2009. The evolution of photoperiod response systems and seasonal GnRH plasticity in birds. Integr. Comp. Biol. 49, 580-589. https://doi.org/10.1093/icb/icp048.
    McGuire, N.L., Bentley, GE., 2010. A functional neuropeptide system in vertebrate gonads: Gonadotropin-inhibitory hormone and its receptor in testes of field caught house sparrow (Passer domesticus). Gen. Comp. Endocrinol. 166, 565-572. https://doi.org/10.1016/j.ygcen.2010.01.010.
    McGuire, N., Ferris, J.K., Arckens, L., Bentley, G.E., Soma, K.K., 2013. Gonadotropin releasing hormone (GnRH) and gonadotropin inhibitory hormone (GnIH) in the songbird hippocampus: regional and sex differences in adult zebra finches. Peptides. 46, 64-75. https://doi.org/10.1016/j.peptides.2013.05.007.
    Meddle, S.L., Wingfield, J.C., Millar, R.P., Deviche, P.J., 2006. Hypothalamic GnRH-I and its precursor during photorefractoriness onset in free-living male Dark-eyed Juncos (Junco hyemalis) of different year classes. Gen. Comp. Endocrinol. 145, 148-156. https://doi.org/10.1016/j.ygcen.2005.08.013.
    Nabi, G., Hao, Y., Liu, X., Sun, Y., Wang, Y., Jiang, C., et al., 2020. Hypothalamic-pituitary-thyroid axis crosstalk with the hypothalamic-pituitary-gonadal axis and metabolic regulation in the Eurasian tree sparrow during mating and non-mating periods. Front. Endocrinol (Lausanne). 11, 303. https://doi.org/10.3389/fendo.2020.00303.
    Nabi, G., Xing, D.N., Sun, Y.F., Zhang, Q., Li, M., Jiang, C., et al., 2021. Coping with extremes: high-altitude sparrows enhance metabolic and thermogenic capacities in the pectoralis muscle and suppress in the liver relative to their lowland counterparts. Gen. Comp. Endocrinol. 313, 113890. https://doi.org/10.1016/j.ygcen.2021.113890.
    Nilsson, J.Å., Råberg, L., 2001. The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia. 128, 187-192. https://doi.org/10.1007/s004420100653.
    Otsuka, S., Namiki, Y., Ichii, O., Hashimoto, Y., Sasaki, N., Endoh, D., et al., 2010. Analysis of factors decreasing testis weight in MRL mice. Mamm. Genome. 21, 153-161. https://doi.org/10.1007/s00335-010-9251-0.
    Ottinger, M.A., Abdelnabi, M., Li, Q., Chen, K., Thompson, N., Harada, N., et al., 2004. The Japanese quail: A model for studying reproductive aging of hypothalamic systems. Exp. Gerontol. 39, 1679-1693. https://doi.org/10.1016/j.exger.2004.06.021.
    Pageau, C., Sonnleitner, J., Tonra, C.M., Shaikh, M., Reudink, M.W., 2021. Evolution of winter molting strategies in European and North American migratory passerines. Ecol. Evol. 11, 13247-13258. https://doi.org/10.1002/ece3.8047.
    Peixoto, J.V., Paula, T.A.R., Balarini, M.K., Matta, S.L.P., Santos, J.A.D., Lima, C.B., et al., 2012. Morphofunctional evaluation of the testicle and the spermatogenic process of adult white-eyed parakeets (Aratinga leucophthalma Muller, 1776) during the different seasons of the year. Anat. Histol. Embryol. 41, 248-255. https://doi.org/10.1111/j.1439-0264.2011.01128.x.
    Perfito, N., Zann, R., Ubuka, T., Bentley, G., Hau, M., 2011. Potential roles for GNIH and GNRH-II in reproductive axis regulation of an opportunistically breeding songbird. Gen. Comp. Endocrinol. 173, 20-26. https://doi.org/10.1016/j.ygcen.2011.04.016.
    Print, C.G., Loveland, K.L., 2000. Germ cell suicide: new insights into apoptosis during spermatogenesis. BioEssays. 22, 423-430. https://doi.org/10.1002/(SICI)1521-1878(200005)22:5<423::AID-BIES4>3.0.CO;2-0. doi: 10.1002/(SICI)1521-1878(200005)22:5<423::AID-BIES4>3.0.CO;2-0
    Rizwan, M.Z., Poling, M.C., Corr, M., Cornes, P.A., Augustine, R.A., Quennell, J.H., et al., 2012. RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology. 153, 3770-3779. https://doi.org/10.1210/en.2012-1133.
    Shil, S.K., Quasem, M.A., Rahman, M.L., 2015. Histological and morphometric analysis of testes of adult quail (Coturnix coturnix japonica) of Bangladesh. Int. J. Morphol. 33, 100-104. https://doi.org/10.4067/S0717-95022015000100017.
    Sibly, R.M., Witt, C.C., Wright, N.A., Venditti, C., Jetz, W., Brown, J.H., 2012. Energetics, lifestyle, and reproduction in birds. Proc. Natl. Acad. Sci. USA. 109, 10937-10941. https://doi.org/10.1073/pnas.1206512109.
    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. https://doi.org/10.1016/j.ygcen.2005.02.019.
    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. Endocrinology. 150, 1826-1833. https://doi.org/10.1210/en.2008-1435.
    Stevenson, T.J., Hahn, T.P., Ball, G.F., 2012. Variation in gonadotrophin-releasing hormone-1 gene expression in the preoptic area predicts transitions in seasonal reproductive state. J. Neuroendocrinol. 24, 267-274. https://doi.org/10.1111/j.1365-2826.2011.02245.x.
    Sun, Y.F., Ren, Z.P., Wu, Y.F., Lei, F.M., Dudley, R., Li, D.M., 2016. Flying high: limits to flight performance by sparrows on the Qinghai-Tibet Plateau. J. Exp. Biol. 219, 3642-3648. https://doi.org/10.1242/jeb.142216.
    Surbhi, R.A., Rani, S., Kumar, V., 2015. 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. 27, 357-369. https://doi.org/10.1111/jne.12274.
    Teo, C.H., Phon, B., Parhar, I., 2021. The role of GnIH in biological rhythms and social behaviors. Front. Endocrinol (Lausanne). 12, 728862. https://doi.org/10.3389/fendo.2021.728862.
    Teruyama, R., Beck, M.M., 2000. Changes in immunoreactivity to anti-cGnRH-I and -II are associated with photostimulated sexual status in male quail. Cell Tissue. Res. 300, 413-426. https://doi.org/10.1007/s004410000218.
    Tsutsui, K., 2009. A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): Biosynthesis, mode of action and functional significance. Prog. neurobiol. 88, 76-88. https://doi.org/10.1016/j.pneurobio.2009.02.003.
    Tsutsui, K., 2016. How to contribute to the progress of neuroendocrinology: new insights from discovering novel neuropeptides and neurosteroids regulating pituitary and brain functions. Gen. Comp. Endocrinol. 227, 3-15. https://doi.org/10.1016/j.ygcen.2015.05.019.
    Tsutsui, K., Ubuka, T., 2020. Discovery of gonadotropin-inhibitory hormone (GnIH), progress in GnIH research on reproductive physiology and behavior and perspective of GnIH research on neuroendocrine regulation of reproduction. Mol. Cell. Endocrinol. 514, 110914. https://doi.org/10.1016/j.mce.2020.110914.
    Tsutsui, K., Ubuka, T., 2021. Gonadotropin-inhibitory hormone (GnIH): A new key neurohormone controlling reproductive physiology and behavior. Front. Neuroendocrinol. 61, 100900. https://doi.org/10.1016/j.yfrne.2021.100900.
    Tsutsui, K., Ukena, K., 2006. Hypothalamic LPXRF-amide peptides in vertebrates: identification, localization and hypophysiotropic activity. Peptides. 27, 1121-1129. https://doi.org/10.1016/j.peptides.2005.06.036.
    Tsutsui, K., Bentley, G., Kriegsfeld, L., Osugi, T., Seong, J.Y., Vaudry, H., 2010a. Discovery and evolutionary history of Gonadotrophin-inhibitory hormone and Kisspeptin: new key neuropeptides controlling reproduction. J. Neuroendocrinol. 22, 716-727. https://doi.org/10.1111/j.1365-2826.2010.02018.x.
    Tsutsui, K., Bentley, G.E., Bedecarrats, G., Osugi, T., Ubuka, T., Kriegsfeld, L.J., 2010b. Gonadotropin inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front. Neuroendocrinol. 31, 284-295. https://doi.org/10.1016/j.yfrne.2010.03.001.
    Tsutsui, K., Ubuka, T., Son, Y.L., Bentley, G.E., Kriegsfeld, L.J., 2015. Contribution of GnIH research to the progress of reproductive neuroendocrinology. Front. Endocrinol (Lausanne). 6, 179. https://doi.org/10.3389/fendo.2015.00179.
    Tsutsui, K., Ubuka, T., Bentley, G.E., Kriegsfeld, L.J., 2012. Gonadotropin-inhibitory hormone (GnIH): discovery, progress and prospect. Gen. Comp. Endocrinol. 177, 305-314. https://doi.org/10.1016/j.ygcen.2012.02.013.
    Ubuka, T., Bentley, G.E., 2009. Identification, localization, and regulation of passerine GnRH-I messenger RNA. J. Endocrinol. 201, 81-87. https://doi.org/10.1677/JOE-08-0508.
    Ubuka, T., Ukena, K., Sharp, P.J., Bentley, G.E., Tsutsui, K., 2006. Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology. 147, 1187-1194. https://doi.org/10.1210/en.2005-1178.
    Ubuka, T., Bentley, G.E., Tsutsui, K., 2013. Neuroendocrine regulation of gonadotropin secretion in seasonally breeding birds. Front. Neurosci. 7, 38. https://doi.org/10.3389/fnins.2013.00038.
    van Gils, J., Absil, P., Grauwels, L., Moons, L., Vandesande, F., Balthazart, J., 1993. Distribution of luteinizing hormone-releasing hormones I and II (LHRH-I and -II) in the quail and chicken brain as demonstrated with antibodies directed against synthetic peptides. J. Comp. Neurol. 334, 304-323. https://doi.org/10.1002/cne.903340211.
    Vézina, F., Salvante, K.G., 2010. Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction. Curr. Zool. 56, 767-792. https://doi.org/10.1654/4406.1.
    Vézina, F., Williams, T.D., 2002. Metabolic costs of egg production in the European starling (Sturnus vulgaris). Physiol. Biochem. Zool. 75, 377-385. https://doi.org/10.1086/343137.
    Vézina, F., Williams, T.D., 2003. Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiol. Biochem. Zool. 76, 716-730. https://doi.org/10.1086/376425.
    Williams, T.D., 2005. Mechanisms underlying the costs of egg production. BioScience. 55, 39-48. https://doi.org/10.1641/0006-3568(2005)055[0039:mutcoe]2.0.co;2.
    Williams, T.D., Ames, C.E., 2004. Top-down regression of the avian oviduct during late oviposition in a small passerine bird. J. Exp. Biol. 207, 263-268. https://doi.org/10.1242/jeb.00740.
    Wingfield, J.C., 2008. Comparative endocrinology, environment and global change. Gen. Comp. Endocrinol. 157, 207-216. https://doi.org/10.1016/j.ygcen.2008.04.017.
    Wolfe, J.D., Terrill, R.S., Johnson, E.I., Powell, L.L., Brandt, R.T., 2021. Ecological and evolutionary significance of molt in lowland Neotropical landbirds. Ornithology. 138, 1-13. https://doi.org/10.1093/ornithology/ukaa073.
    Young, K.A., Nelson, R.J., 2001. Mediation of seasonal testicular regression by apoptosis. Reproduction. 122, 677-685. https://doi.org/10.1530/rep.0.1220677.
    Young, K.A., Ball, G.F., Nelson, R.J., 2001. Photoperiod-induced testicular apoptosis in European starlings (Sturnus vulgaris). Biol. Reprod. 64, 706-713. https://doi.org/10.1095/biolreprod64.2.706.
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(4)  / Tables(2)

    Article Metrics

    Article views (30) PDF downloads(0) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint