Molecular and Neuroendocrine Mechanisms of Avian Seasonal Reproduction

  • T. Katherine Tamai
  • Takashi YoshimuraEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1001)


Animals living outside tropical zones experience seasonal changes in the environment and accordingly, adapt their physiology and behavior in reproduction, molting, and migration. Subtropical birds are excellent models for the study of seasonal reproduction because of their rapid and dramatic response to changes in photoperiod. For example, testicular weight typically changes by more than a 100-fold. In birds, the eyes are not necessary for seasonal reproduction, and light is instead perceived by deep brain photoreceptors. Functional genomic analysis has revealed that long day (LD)-induced thyrotropin from the pars tuberalis of the pituitary gland causes local thyroid hormone (TH) activation within the mediobasal hypothalamus. This local bioactive TH, triiodothyronine (T3), appears to regulate seasonal gonadotropin-releasing hormone (GnRH) secretion through morphological changes in neuro-glial interactions. GnRH, in turn, stimulates gonadotropin secretion and hence, gonadal development under LD conditions. In marked contrast, low temperatures accelerate short day (SD)-induced testicular regression in winter. Interestingly, low temperatures increase circulating levels of T3 to support adaptive thermogenesis, but this induction of T3 also triggers the apoptosis of germ cells by activating genes involved in metamorphosis. This apparent contradiction in the role of TH has recently been clarified. Central activation of TH during spring results in testicular growth, while peripheral activation of TH during winter regulates adaptive thermogenesis and testicular regression.


Photoperiodism Circadian rhythm Mediobasal hypothalamus Pars tuberalis Thyrotropin Thyroid hormone Deep brain photoreceptor Opsin 


  1. Abe T, Suzuki T, Unno M, Tokui T, Ito S. Thyroid hormone transporters: recent advances. Trends Endocrinol Metab. 2002;13:215–20.CrossRefPubMedGoogle Scholar
  2. Bailey MJ, Cassone VM. Melanopsin expression in the chick retina and pineal gland. Brain Res Mol Brain Res. 2005;134:345–8.CrossRefPubMedGoogle Scholar
  3. Balsalobre A. Clock genes in mammalian peripheral tissues. Cell Tissue Res. 2002;309:193–9.CrossRefPubMedGoogle Scholar
  4. Benoit J. Le role des yeux dans l’action stimulante de la lumière sur le developpement testiculaire chez le canard. C R Soc Biol (Paris). 1935;118:669–71.Google Scholar
  5. Bernal J. Action of thyroid hormone in brain. J Endocrinol Invest. 2002;25:268–88.CrossRefPubMedGoogle Scholar
  6. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295:1070–3.CrossRefPubMedGoogle Scholar
  7. Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, Zatz M, Tosini G, Liu C, Korf HW, Iuvone PM, Provencio I. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J Neurochem. 2005;92:158–70.CrossRefPubMedGoogle Scholar
  8. Davies DT, Follett BK. The neuroendocrine control of gonadotrophin release in the Japanese quail. II. The role of the anterior hypothalamus. Proc R Soc Lond B. 1975;191:303–15.CrossRefPubMedGoogle Scholar
  9. Davies WI, Turton M, Peirson SN, Follett BK, Halford S, Garcia-Fernandez JM, Sharp PJ, Hankins MW, Foster RG. Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol Lett. 2012;8:291–4.CrossRefPubMedGoogle Scholar
  10. Dawson A, King VM, Bentley GE, Ball GF. Photoperiodic control of seasonality in birds. J Biol Rhythms. 2001;16:365–80.CrossRefPubMedGoogle Scholar
  11. Ebihara S, Kawamura H. The role of the pineal organ and the suprachiasmatic nucleus in the control of circadian locomotor rhythms in the Java sparrow, Padda oryzivora. J Comp Physiol A. 1981;141:207–14.CrossRefGoogle Scholar
  12. Follett BK, Maung SL. Rate of testicular maturation, in relation to gonadotrophin and testosterone levels, in quail exposed to various artificial photoperiods and to natural daylengths. J Endocrinol. 1978;78:267–80.CrossRefPubMedGoogle Scholar
  13. Follett BK, Sharp PJ. Circadian rhythmicity in photoperiodically induced gonadotrophin release and gonadal growth in the quail. Nature. 1969;223:968–71.CrossRefPubMedGoogle Scholar
  14. Follett BK, King VM, Meddle SL. Rhythms and photoperiodism in birds. In: Lumsden PJ, Miller AJ, editors. Biological rhythms and photoperiodism in plants. Oxford: Biostatistics Scientific; 1998. p. 231–42.Google Scholar
  15. Foster RG, Follett BK. The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J Comp Physiol A. 1985;157:519–28.CrossRefGoogle Scholar
  16. Foster RG, Follett BK, Lythgoe JN. Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail. Nature. 1985;313:50–2.CrossRefPubMedGoogle Scholar
  17. Foster RG, Korf HW, Schalken JJ. Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res. 1987;248:161–7.CrossRefPubMedGoogle Scholar
  18. Furlow JD, Neff ES. A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends Endocrionol Metab. 2006;17:40–7.CrossRefGoogle Scholar
  19. Garner WW, Allard HA. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res. 1920;18:553–606.Google Scholar
  20. Gwinner E, Hau H, Heigl S. Melatonin: generation and modification of avian circadian rhythms. Brain Res Bull. 1997;44:439–44.CrossRefPubMedGoogle Scholar
  21. Hagenbuch B, Meier PJ. Organic anion transporting polypeptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Eur J Physiol. 2004;447:653–65.CrossRefGoogle Scholar
  22. Hahn TP, MacDougall-Shackleton SA. Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos Trans R Soc B. 2008;363:267–86.CrossRefGoogle Scholar
  23. Halford S, Pires SS, Turton M, Zheng L, Gonzalez-Menendez I, Davies WL, Peirson SN, Garcia-Fernandez JM, Hankins MW, Foster RG. VA opsin-based photoreceptors in the hypothalamus of birds. Curr Biol. 2009;19:1396–402.CrossRefPubMedGoogle Scholar
  24. Homma K, Ohta M, Sakakibara Y. Photoinducible phase of the Japanese quail detected by direct stimulation of the brain. In: Suda M, Hayaishi O, Nakagawa H, editors. Biological rhythms and their central mechanism. Amsterdam: Elsevier; 1979. p. 85–94.Google Scholar
  25. Ikegami K, Katou Y, Higashi K, Yoshimura T. Localization of circadian clock protein BMAL1 in the photoperiodic signal transduction machinery in Japanese quail. J Comp Neurol. 2009;517:397–404.CrossRefPubMedGoogle Scholar
  26. Ikegami K, Liao XH, Hoshino Y, Ono H, Ota W, Ito Y, Nishiwaki-Ohkawa T, Sato C, Kitajima K, Iigo M, Shigeyoshi Y, Yamada M, Murata Y, Refetoff S, Yoshimura T. Tissue-specific post-translational modification allows functional targeting of thyrotropin. Cell Rep. 2014;9:1–9.CrossRefGoogle Scholar
  27. Ikegami K, Atsumi Y, Yorinaga E, Ono H, Murayama I, Nakane Y, Ota W, Arai N, Tega A, Iigo M, Darras VM, Tsutsui K, Hayashi Y, Yoshida S, Yoshimura T. Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression. Endocrinology. 2015;156:647–59.CrossRefPubMedGoogle Scholar
  28. Juss TS, Meddle SL, Servant RS, King VM. Melatonin and photoperiodic time measurement in Japanese quail (Coturnix coturnix japonica). Proc R Soc Lond B Biol Sci. 1993;254:21–8.CrossRefGoogle Scholar
  29. Kang SW, Leclerc B, Kosonsiriluk S, Mauro LJ, Iwasawa A, El Halawani ME. Melanopsin expression in dopamine–melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds. Neuroscience. 2010;170:200–13.CrossRefPubMedGoogle Scholar
  30. Konishi H, Foster RG, Follett BK. Evidence for a daily rhythmicity in the acute release of LH in response to electrical stimulation in the Japanese quail. J Comp Physiol A Sens Neural Behav Physiol. 1987;161:315–9.CrossRefGoogle Scholar
  31. Lamb TD. Evolution of vertebrate retinal photoreception. Phil Trans R Soc B. 2009;364:2911–24.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lofts B, Murton RK, Westwood NJ. Photoresponses of the Woodpigeon Columba palumbus in relation to the breeding season. Ibis. 1967;109:338–51.CrossRefGoogle Scholar
  33. MacDougall-Shackleton SA, Stevenson TJ, Watts HE, Pereyra ME, Hahn TP. The evolution of photoperiod response systems and seasonal GnRH plasticity in birds. Integr Comp Biol. 2009;49:580–9.CrossRefPubMedGoogle Scholar
  34. Marcovitch S. Plant lice and light exposure. Science. 1923;58:537–8.CrossRefPubMedGoogle Scholar
  35. Max M, McKinnon PJ, Seidenman KJ, Barrett RK, Applebury ML, Takahashi JS, Margolskee RF. Pineal opsin: a nonvisual opsin expressed in chick pineal. Science. 1995;267:1502–6.CrossRefPubMedGoogle Scholar
  36. Meddle SL, Follett BK. Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neurosci. 1997;17:8909–18.PubMedGoogle Scholar
  37. Menaker M. Extraretinal light perception in the sparrow. I. Entrainment of the biological clock. Proc Natl Acad Sci U S A. 1968;59:414–21.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Menaker M, Roberts R, Elliott J, Underwood H. Extraretinal light perception in the sparrow. III. The eyes do not participate in photoperiodic photoreception. Proc Natl Acad Sci U S A. 1970;67:320–5.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nakane Y, Yoshimura T. Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates. Front Neurosci. 2014;8:115.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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;107:15264–8.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, Uesaka M, Kimijima M, Hashimoto R, Arai N, Suga T, Kosuge K, Abe T, Maeda R, Senga T, Amiya N, Azuma T, Amano M, Abe H, Yamamoto N, Yoshimura T. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun. 2013;4:2108.CrossRefPubMedGoogle Scholar
  42. Nakane Y, Shimmura T, Abe H, Yoshimura T. Intrisic photosensitivity of a deep brain photoreceptor. Curr Biol. 2014;24:R596–7.CrossRefPubMedGoogle Scholar
  43. Nakao N, Takagi T, Iigo M, Tsukamoto T, Yasuo S, Masuda T, Yanagisawa T, Ebihara S, Yoshimura T. Possible involvement of organic anion transporting polypeptide 1c1 in the photoperiodic response of gonads in birds. Endocrinology. 2006;147:1067–73.CrossRefPubMedGoogle Scholar
  44. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, Ueda HR, Yoshimura T. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature. 2008;452:317–22.CrossRefPubMedGoogle Scholar
  45. Nicholls TJ, Follett BK, Robinson JE. A photoperiodic response in gonadectomized Japanese quail exposed to a single long day. J Endocrinol. 1983;97:121–6.CrossRefPubMedGoogle Scholar
  46. Nicholls TJ, Goldsmith AR, Dawson A. Photorefractoriness in birds and comparison with mammals. Physiol Rev. 1988;68:133–76.PubMedGoogle Scholar
  47. Oishi T, Konishi T. Effects of photoperiod and temperature on testicular and thyroid activity of the Japanese quail. Gen Comp Endocrinol. 1978;36:250–4.CrossRefPubMedGoogle Scholar
  48. Okano T, Yoshizawa T, Fukada Y. Pinopsin is a chicken pineal photoreceptive molecule. Nature. 1994;372:94–7.CrossRefPubMedGoogle Scholar
  49. Oliver J, Bayle JD. Brain photoreceptors for the photoinduced testicular response in birds. Experientia. 1982;38:1020–9.CrossRefGoogle Scholar
  50. Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, Ebihara S, Korf HW, Yoshimura T. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci U S A. 2008;105:18238–42.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ono H, Nakao N, Yamamura T, Kinoshita K, Mizutami M, Namikawa T, Iigo M, Ebihara S, Yoshimura T. Red jungle fowl (Gallus gallus) as a model for studying the molecular mechanism of seasonal reproduction. Anim Sci J. 2009;80:328–32.CrossRefPubMedGoogle Scholar
  52. Pearce EN. Thyroid hormone and obesity. Curr Opin Endocrinol Diabetes Obes. 2012;19:408–13.CrossRefPubMedGoogle Scholar
  53. Perfito N, Jeong SY, Silverin B, Calisi RM, Bentley GE, Hau M. Anticipating spring: wild populations of great tits (Parus major) differ in expression of key genes for photoperiodic time measurement. PLoS One. 2012;7:e34997.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, Beauvillain JC. Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience. 1999;94:809–19.CrossRefPubMedGoogle Scholar
  55. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature. 2002;418:935–41.CrossRefPubMedGoogle Scholar
  56. Rowan W. Relation of light to bird migration and developmental changes. Nature. 1925;115:494–5.CrossRefGoogle Scholar
  57. Sharp PJ, Follett BK. The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinol. 1969;5:205–18.CrossRefGoogle Scholar
  58. Silva JE. Thermogenic mechanisms and their hormonal regulation. Physiol Rev. 2006;86:435–64.CrossRefPubMedGoogle Scholar
  59. Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN. Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res. 1988;253:189–98.CrossRefPubMedGoogle Scholar
  60. Siopes TD, Wilson WO. Extraocular modification of photoreception in intact and pinealectomized coturnix. Poult Sci. 1974;53:2035–41.CrossRefPubMedGoogle Scholar
  61. Steele CT, Zivkovic BD, Siopes T, Underwood H. Ocular clocks are tightly coupled and act as pacemakers in the circadian system of Japanese quail. Am J Physiol Regul Integr Comp Physiol. 2003;284:R208–18.CrossRefPubMedGoogle Scholar
  62. Stevenson TJ, Ball GF. Disruption of neuropsin mRNA expression via RNA interference facilitates the photoinduced increase in thyrotropin-stimulating subunit β in birds. Eur J Neurosci. 2012;36:2859–65.CrossRefPubMedGoogle Scholar
  63. Stevenson TJ, Hahn TP, MacDougall-Shackleton SA, Ball GF. Gonadotropin-releasing hormone plasticity: a comparative perspective. Front Neuroendocrionol. 2012;33:287–300.CrossRefGoogle Scholar
  64. Takahashi JS, Menaker M. Role of the suprachiasmatic nucleus in the circadian system of the house sparrow. J Neurosci. 1982;2:815–28.PubMedGoogle Scholar
  65. Tarttelin EE, Bellingham J, Hankins MW, Foster RG, Lucas RJ. Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue. FEBS Lett. 2003;554:410–6.CrossRefPubMedGoogle Scholar
  66. Tomonari S, Takagi A, Akamatsu S, Noji S, Ohuchi H. A non-canonical photopigment, melanopsin, is expressed in the differentiating ganglion, horizontal, and bipolar cells of the chicken retina. Dev Dyn. 2005;234:783–90.CrossRefPubMedGoogle Scholar
  67. Tomonari S, Takagi A, Noji S, Ohuchi H. Expression pattern of the melanopsin-like (cOpn4m) and VA opsin-like genes in the developing chicken retina and neural tissues. Gene Expr Patterns. 2007;7:746–53.CrossRefPubMedGoogle Scholar
  68. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun. 2000;275:661–7.CrossRefPubMedGoogle Scholar
  69. Ubuka T, Bentley GE, Ukena K, Wingfield JC, Tsutsui K. Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc Natl Acad Sci U S A. 2005;102:3052–7.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Ubuka T, Ukena K, Sharp PJ, Bentley GE, Tsutsui K. Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology. 2006;147:1187–94.CrossRefPubMedGoogle Scholar
  71. Vigh B, Vigh-Teichmann I. Actual problems of the cerebrospinal fluid-contacting neurons. Microsc Res Tech. 1998;41:57–83.CrossRefPubMedGoogle Scholar
  72. von Frisch K. Beitrage zur Physiologie der Pigmentzellen in der Fischhaut. Pfluger’s Archiv fűr die Gesamte Physiologie des Menschen und der Tiere. 1911;138:319–87.CrossRefGoogle Scholar
  73. Wada M. Low temperature and short days together induce thyroid activation and suppression of LH release in Japanese quail. Gen Comp Endocrinol. 1993;90:355–63.CrossRefPubMedGoogle Scholar
  74. Wada Y, Okano T, Adachi A, Ebihara S, Fukada Y. Identification of rhodopsin in the pigeon deep brain. FEBS Lett. 1998;424:53–6.CrossRefPubMedGoogle Scholar
  75. Watanabe T, Yamamura T, Watanabe M, Yasuo S, Nakao N, Dawson A, Ebihara S, Yoshimura T. 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:R568–72.CrossRefPubMedGoogle Scholar
  76. Waung JA, Bassett JH, Williams GR. Thyroid hormone metabolism in skeletal development and adult bone maintenance. Trends Endocrinol Metab. 2012;23:155–62.CrossRefPubMedGoogle Scholar
  77. Yamamura T, Hirunagi K, Ebihara S, Yoshimura T. Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology. 2004;145:4264–7.CrossRefPubMedGoogle Scholar
  78. Yamamura T, Yasuo S, Hirunagi K, Ebihara S, Yoshimura T. T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res. 2006;324:175–9.CrossRefPubMedGoogle Scholar
  79. Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y. Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc Natl Acad Sci U S A. 2010;107:22084–9.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000;288:682–5.CrossRefPubMedGoogle Scholar
  81. Yasuo S, Watanabe M, Okabayashi N, Ebihara S, Yoshimura T. Circadian clock genes and photoperiodism: comprehensive analysis of clock gene expression in the mediobasal hypothalamus, the suprachiasmatic nucleus, and the pineal gland of Japanese quail under various light schedules. Endocrinology. 2003;144:3742–8.CrossRefPubMedGoogle Scholar
  82. Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK, Ebihara S, Yoshimura T. The reciprocal switching of two thyroid hormone-activating and -inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology. 2005;146:2551–4.CrossRefPubMedGoogle Scholar
  83. Yasuo S, Yoshimura T, Ebihara S, Kolf HW. Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J Neurosci. 2009;29:2885–9.CrossRefPubMedGoogle Scholar
  84. Yoshimura T, Yasuo S, Suzuki Y, Makino E, Yokota Y, Ebihara S. Identification of the suprachiasmatic nucleus in birds. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1185–9.PubMedGoogle Scholar
  85. 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;426:178–81.CrossRefPubMedGoogle Scholar
  86. Young MW, Kay SA. Time zones: a comparative genetics of circadian clocks. Nat Rev Genet. 2001;2:702–15.CrossRefPubMedGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.Institute of Transformative Bio-Molecules (WPI-ITbM)Nagoya UniversityNagoyaJapan
  2. 2.Laboratory of Animal Physiology, Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  3. 3.Avian Bioscience Research Center, Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  4. 4.National Institute for Basic BiologyOkazakiJapan

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