1932

Abstract

Organisms use changes in photoperiod for seasonal reproduction to maximize the survival of their offspring. Birds have sophisticated seasonal mechanisms and are therefore excellent models for studying these phenomena. Birds perceive light via deep-brain photoreceptors and long day–induced thyroid-stimulating hormone (TSH, thyrotropin) in the pars tuberalis of the pituitary gland (PT), which cause local thyroid hormone activation within the mediobasal hypothalamus. The local bioactive thyroid hormone controls seasonal gonadotropin-releasing hormone secretion and subsequent gonadotropin secretion. In mammals, the eyes are believed to be the only photoreceptor organ, and nocturnal melatonin secretion triggers an endocrine signal that communicates information about the photoperiod to the PT to regulate TSH. In contrast, in Salmonidae fish the input pathway to the neuroendocrine output pathway appears to be localized in the saccus vasculosus. Thus, comparative analysis is an effective way to uncover the universality and diversity of fundamental traits in various organisms.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-020518-115216
2019-02-15
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/animal/7/1/annurev-animal-020518-115216.html?itemId=/content/journals/10.1146/annurev-animal-020518-115216&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Garner WW, Allard HA 1920. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J. Agric. Res. 18:553–606
    [Google Scholar]
  2. 2.  Dawson A, King VM, Bentley GE, Ball GF 2001. Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16:365–80
    [Google Scholar]
  3. 3.  Watanabe M, Yasuo S, Watanabe T, Yamamura T, Nakao N et al. 2004. Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology 145:1546–49
    [Google Scholar]
  4. 4.  Young KA, Ball GF, Nelson RJ 2001. Photoperiod-induced testicular apoptosis in European starlings (Sturnus vulgaris). Biol. Reprod. 64:706–13
    [Google Scholar]
  5. 5.  Elliott JA 1976. Circadian rhythms and photoperiodic time measurement in mammals. Fed. Proc. 35:2339–46
    [Google Scholar]
  6. 6.  Goldman BD 2001. Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J. Biol. Rhythms 16:283–301
    [Google Scholar]
  7. 7.  Follett BK, Maung SL 1978. Rate of testicular maturation, in relation to gonadotrophin and testosterone levels, in quail exposed to various artificial photoperiods and to natural daylengths. J. Endocrinol. 78:267–80
    [Google Scholar]
  8. 8.  Pittendrigh CS, Minis DH 1964. The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am. Nat. 98:261–99
    [Google Scholar]
  9. 9.  Pittendrigh CS 1972. Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. PNAS 69:2734–37
    [Google Scholar]
  10. 10.  Okano T, Yoshizawa T, Fukada Y 1994. Pinopsin is a chicken pineal photoreceptive molecule. Nature 372:94–97
    [Google Scholar]
  11. 11.  Von Frisch K 1911. Beitrage zur physiologie der pigmentzellen in der fischhaut. Pfluger's Archiv. Gesammte Physiol. Menschen Tiere 138:319–87
    [Google Scholar]
  12. 12.  Benoit J 1935. Le role des yeux dans l'action stimulante de la lumiere sure le developpement testiulaire chez le canard. C. R. Soc. Biol. 118:669–71
    [Google Scholar]
  13. 13.  Oliver J, Bayle JD 1982. Brain photoreceptors for the photoinduced testicular response in birds. Experientia 38:1020–29
    [Google Scholar]
  14. 14.  Siopes TD, Wilson WO 1974. Extraocular modification of photoreception in intact and pinealectomized coturnix. Poult. Sci. 53:2035–41
    [Google Scholar]
  15. 15.  Menaker M, Roberts R, Elliott J, Underwood H 1970. Extraretinal light perception in the sparrow. III. The eyes do not participate in photoperiodic photoreception. PNAS 67:320–25
    [Google Scholar]
  16. 16.  Homma K, Ohta M, Sakakibara Y 1979. Photoinducible phase of the Japanese quail detected by direct stimulation of the brain. Biological Rhythms and Their Central Mechanism M Suda, O Hayaishi, H Nakagawa 85–94 Amsterdam: Elsevier
    [Google Scholar]
  17. 17.  Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN 1988. Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res 253:189–98
    [Google Scholar]
  18. 18.  Wada Y, Okano T, Adachi A, Ebihara S, Fukada Y 1998. Identification of rhodopsin in the pigeon deep brain. FEBS Lett 424:53–56
    [Google Scholar]
  19. 19.  Vigh B, Vigh-Teichmann I 1998. Actual problems of the cerebrospinal fluid-contacting neurons. Microsc. Res. Tech. 41:57–83
    [Google Scholar]
  20. 20.  Foster RG, Korf HW, Schalken JJ 1987. Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res 248:161–67
    [Google Scholar]
  21. 21.  Bailey MJ, Cassone VM 2005. Melanopsin expression in the chick retina and pineal gland. Brain Res. Mol. Brain Res. 134:345–48
    [Google Scholar]
  22. 22.  Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R et al. 2005. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J. Neurochem. 92:158–70
    [Google Scholar]
  23. 23.  Kang SW, Leclerc B, Kosonsiriluk S, Mauro LJ, Iwasawa A, El Halawani ME 2010. Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds. Neuroscience 170:200–13
    [Google Scholar]
  24. 24.  Tomonari S, Takagi A, Akamatsu S, Noji S, Ohuchi H 2005. A non-canonical photopigment, melanopsin, is expressed in the differentiating ganglion, horizontal, and bipolar cells of the chicken retina. Dev. Dyn. 234:783–90
    [Google Scholar]
  25. 25.  Tomonari S, Takagi A, Noji S, Ohuchi H 2007. Expression pattern of the melanopsin-like (cOpn4m) and VA opsin-like genes in the developing chicken retina and neural tissues. Gene Expr. Patterns 7:746–53
    [Google Scholar]
  26. 26.  Davies WI, Turton M, Peirson SN, Follett BK, Halford S et al. 2012. Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol. Lett. 8:291–94
    [Google Scholar]
  27. 27.  Halford S, Pires SS, Turton M, Zheng L, González-Menéndez I et al. 2009. VA opsin-based photoreceptors in the hypothalamus of birds. Curr. Biol. 19:1396–402
    [Google Scholar]
  28. 28.  Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S et al. 2010. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. PNAS 107:15264–68
    [Google Scholar]
  29. 29.  Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y 2010. Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. PNAS 107:22084–89
    [Google Scholar]
  30. 30.  Foster RG, Follett BK 1985. The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J. Comp. Physiol. A 157:519–28
    [Google Scholar]
  31. 31.  Foster RG, Follett BK, Lythgoe JN 1985. Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail. Nature 313:50–52
    [Google Scholar]
  32. 32.  Sharp PJ, Follett BK 1969. The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology 5:205–18
    [Google Scholar]
  33. 33.  Ebihara S, Kawamura H 1981. 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 141:207–14
    [Google Scholar]
  34. 34.  Menaker M 1968. Extraretinal light perception in the sparrow: I. Entrainment of the biological clock. PNAS 59:414–21
    [Google Scholar]
  35. 35.  Steele CT, Zivkovic BD, Siopes T, Underwood H 2003. Ocular clocks are tightly coupled and act as pacemakers in the circadian system of Japanese quail. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284:R208–18
    [Google Scholar]
  36. 36.  Takahashi JS, Menaker M 1982. Role of the suprachiasmatic nucleus in the circadian system of the house sparrow. J. Neurosci. 2:815–28
    [Google Scholar]
  37. 37.  Yoshimura T, Yasuo S, Suzuki Y, Makino E, Yokota Y, Ebihara S 2001. Identification of the suprachiasmatic nucleus in birds. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280:R1185–89
    [Google Scholar]
  38. 38.  Davies DT, Follett BK 1975. The neuroendocrine control of gonadotrophin release in the Japanese quail. II. The role of the anterior hypothalamus. Proc. R. Soc. Lond. B 191:303–15
    [Google Scholar]
  39. 39.  Arendt J 1995. Melatonin and the Mammalian Pineal Gland London: Chapman & Hall
  40. 40.  Reiter RJ 1980. The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev. 1:109–31
    [Google Scholar]
  41. 41.  Whitfield-Rucker MG, Cassone VM 1996. Melatonin binding in the house sparrow song control system: sexual dimorphism and the effect of photoperiod. Horm. Behav. 30:528–37
    [Google Scholar]
  42. 42.  Bentley GE, Van't Hof TJ, Ball GF 1999. Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. PNAS 96:4674–79
    [Google Scholar]
  43. 43.  Wang G, Harpole CE, Trivedi AK, Cassone VM 2012. Circadian regulation of bird song, call, and locomotor behavior by pineal melatonin in the zebra finch. J. Biol. Rhythms 27:145–55
    [Google Scholar]
  44. 44.  Juss TS, Meddle SL, Servant RS, King VM 1993. Melatonin and photoperiodic time measurement in Japanese quail (Coturnix coturnix japonica). Proc. R. Soc. Lond. B 254:21–28
    [Google Scholar]
  45. 45.  Gwinner E, Hau H, Heigl S 1997. Melatonin: generation and modification of avian circadian rhythms. Brain Res. Bull. 44:439–44
    [Google Scholar]
  46. 46.  Bentley GE 2001. Unraveling the enigma: the role of melatonin in seasonal processes in birds. Microsc. Res. Tech. 53:63–71
    [Google Scholar]
  47. 47.  Follett BK, King VM, Meddle SL 1998. Rhythms and photoperiodism in birds. Biological Rhythms and Photoperiodism in Plants PJ Lumsden, AJ Miller 231–42 Oxford: Biostat. Sci
    [Google Scholar]
  48. 48.  Konishi H, Foster RG, Follett BK 1987. Evidence for a daily rhythmicity in the acute release of LH in response to electrical stimulation in the Japanese quail. J. Comp. Physiol. A 161:315–19
    [Google Scholar]
  49. 49.  Meddle SL, Follett BK 1997. Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J. Neurosci. 17:8909–18
    [Google Scholar]
  50. 50.  Follett BK, Sharp PJ 1969. Circadian rhythmicity in photoperiodically induced gonadotrophin release and gonadal growth in the quail. Nature 223:968–71
    [Google Scholar]
  51. 51.  Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T et al. 2003. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426:178–81
    [Google Scholar]
  52. 52.  Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK et al. 2005. The reciprocal switching of two thyroid hormone-activating and -inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology 146:2551–54
    [Google Scholar]
  53. 53.  Watanabe T, Yamamura T, Watanabe M, Yasuo S, Nakao N et al. 2007. 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. 292:R568–72
    [Google Scholar]
  54. 54.  Ono H, Nakao N, Yamamura T, Kinoshita K, Mizutani M et al. 2009. Red jungle fowl (Gallus gallus) as a model for studying the molecular mechanism of seasonal reproduction. Anim. Sci. J. 80:328–32
    [Google Scholar]
  55. 55.  Yamamura T, Hirunagi K, Ebihara S, Yoshimura T 2004. Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology 145:4264–67
    [Google Scholar]
  56. 56.  Prevot V, Croix D, Bouret S, Dutoit S, Tramu G et al. 1999. 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 94:809–19
    [Google Scholar]
  57. 57.  Yamamura T, Yasuo S, Hirunagi K, Ebihara S, Yoshimura T 2006. T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res 324:175–79
    [Google Scholar]
  58. 58.  Abe T, Suzuki T, Unno M, Tokui T, Ito S 2002. Thyroid hormone transporters: recent advances. Trends Endocrinol. Metab. 13:215–20
    [Google Scholar]
  59. 59.  Hagenbuch B, Meier PJ 2004. Organic anion transporting polypeptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Eur. J. Physiol. 447:653–65
    [Google Scholar]
  60. 60.  Nakao N, Takagi T, Iigo M, Tsukamoto T, Yasuo S et al. 2006. Possible involvement of organic anion transporting polypeptide 1c1 in the photoperiodic response of gonads in birds. Endocrinology 147:1067–73
    [Google Scholar]
  61. 61.  Nicholls TJ, Follett BK, Robinson JE 1983. A photoperiodic response in gonadectomized Japanese quail exposed to a single long day. J. Endocrinol. 97:121–26
    [Google Scholar]
  62. 62.  Nakao N, Ono H, Yamamura T, Anraku T, Takagi T et al. 2008. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452:317–22
    [Google Scholar]
  63. 63.  Oishi T, Konishi T 1978. Effects of photoperiod and temperature on testicular and thyroid activity of the Japanese quail. Gen. Comp. Endocrinol. 36:250–54
    [Google Scholar]
  64. 64.  Wada M 1993. Low temperature and short days together induce thyroid activation and suppression of LH release in Japanese quail. Gen. Comp. Endocrinol. 90:355–63
    [Google Scholar]
  65. 65.  Ikegami K, Atsumi Y, Yorinaga E, Ono H, Murayama I et al. 2015. Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression. Endocrinology 156:647–59
    [Google Scholar]
  66. 66.  Furlow JD, Neff ES 2006. A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends Endocrinol. Metab. 17:40–47
    [Google Scholar]
  67. 67.  Legan SJ, Karsch FJ 1983. Importance of retinal photoreceptors to the photoperiodic control of seasonal breeding in the ewe. Biol. Reprod. 29:316–25
    [Google Scholar]
  68. 68.  Hazlerigg DG, Ebling FJ, Johnston JD 2005. Photoperiod differentially regulates gene expression rhythms in the rostral and caudal SCN. Curr. Biol. 15:R449–50
    [Google Scholar]
  69. 69.  Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K 2007. Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. PNAS 104:7664–69
    [Google Scholar]
  70. 70.  Naito E, Watanabe T, Tei H, Yoshimura T, Ebihara S 2008. Reorganization of the suprachiasmatic nucleus coding for day length. J. Biol. Rhythms 23:140–49
    [Google Scholar]
  71. 71.  Nuesslein-Hildesheim B, O'Brien JA, Ebling FJ, Maywood ES, Hastings MH 2000. The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the Siberian hamster encodes both daily and seasonal time. Eur. J. Neurosci. 12:2856–64
    [Google Scholar]
  72. 72.  Sosniyenko S, Hut RA, Daan S, Sumová A 2009. Influence of photoperiod duration and light-dark transitions on entrainment of Per1 and Per2 gene and protein expression in subdivisions of the mouse suprachiasmatic nucleus. Eur. J. Neurosci. 30:1802–14
    [Google Scholar]
  73. 73.  Sumová A, Jác M, Sládek M, Sauman I, Illnerová H 2003. Clock gene daily profiles and their phase relationship in the rat suprachiasmatic nucleus are affected by photoperiod. J. Biol. Rhythms 18:134–44
    [Google Scholar]
  74. 74.  Tournier BB, Menet JS, Dardente H, Poirel VJ, Malan A et al. 2003. Photoperiod differentially regulates clock genes’ expression in the suprachiasmatic nucleus of Syrian hamster. Neuroscience 118:317–22
    [Google Scholar]
  75. 75.  Brown TM, Piggins HD 2009. Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod. J. Biol. Rhythms 24:44–54
    [Google Scholar]
  76. 76.  VanderLeest HT, Houben T, Michel S, Deboer T, Albus H et al. 2007. Seasonal encoding by the circadian pacemaker of the SCN. Curr. Biol. 17:468–73
    [Google Scholar]
  77. 77.  Moenter SM, Woodfill CJ, Karsch FJ 1991. Role of the thyroid gland in seasonal reproduction: Thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes. Endocrinology 128:1337–44
    [Google Scholar]
  78. 78.  Dawson A 1993. Thyroidectomy progressively renders the reproductive system of starlings (Sturnus vulgaris) unresponsive to changes in daylength. J. Endocrinol. 139:51–55
    [Google Scholar]
  79. 79.  Dawson A 1998. Thyroidectomy of house sparrows (Passer domesticus) prevents photo-induced testicular growth but not the increased hypothalamic gonadotrophin-releasing hormone. Gen. Comp. Endocrinol. 110:196–200
    [Google Scholar]
  80. 80.  Parkinson TJ, Follett BK 1995. Thyroidectomy abolishes seasonal testicular cycles of Soay rams. Proc. Biol. Sci. 259:1–6
    [Google Scholar]
  81. 81.  Follett BK, Nicholls TJ 1985. Influences of thyroidectomy and thyroxine replacement on photoperiodically controlled reproduction in quail. J. Endocrinol. 107:211–21
    [Google Scholar]
  82. 82.  Goldsmiths AR, Nicholls TJ 1992. Thyroxine effects upon reproduction, prolactin secretion and plumage moult in thyroidectomised European starlings Sturnus vulgaris.Ornis. . Scand 23:398–404
    [Google Scholar]
  83. 83.  Wilson FE, Reinert BD 2000. Thyroid hormone acts centrally to programme photostimulated male American tree sparrows (Spizella arborea). J. Neuroendocrinol. 12:87–95
    [Google Scholar]
  84. 84.  Barrett P, Ebling FJ, Schuhler S, Wilson D, Ross AW et al. 2007. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 148:3608–17
    [Google Scholar]
  85. 85.  Freeman DA, Teubner BJ, Smith CD, Prendergast BJ 2007. Exogenous T3 mimics long day lengths in Siberian hamsters. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292:R2368–72
    [Google Scholar]
  86. 86.  Herwig A, Wilson D, Logie TJ, Boelen A, Morgan PJ et al. 2009. Photoperiod and acute energy deficits interact on components of the thyroid hormone system in hypothalamic tanycytes of the Siberian hamster. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296:R1307–15
    [Google Scholar]
  87. 87.  Revel FG, Saboureau M, Pévet P, Mikkelsen JD, Simonneaux V 2006. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 147:4680–87
    [Google Scholar]
  88. 88.  Yasuo S, Yoshimura T, Ebihara S, Korf HW 2007. Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology 148:4385–92
    [Google Scholar]
  89. 89.  Ross AW, Helfer G, Russell L, Darras VM, Morgan PJ 2011. Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of F344 rats. PLOS ONE 6:e21351
    [Google Scholar]
  90. 90.  Yasuo S, Watanabe M, Iigo M, Nakamura TJ, Watanabe T et al. 2007. Differential response of type 2 deiodinase gene expression to photoperiod between photoperiodic Fischer 344 and nonphotoperiodic Wistar rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292:R1315–19
    [Google Scholar]
  91. 91.  Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y et al. 2008. Involvement of thyrotropin in photoperiodic signal transduction in mice. PNAS 105:18238–42
    [Google Scholar]
  92. 92.  Yasuo S, Nakao N, Ohkura S, Iigo M, Hagiwara S et al. 2006. Long-day suppressed expression of type 2 deiodinase gene in the mediobasal hypothalamus of the Saanen goat, a short-day breeder: implication for seasonal window of thyroid hormone action on reproductive neuroendocrine axis. Endocrinology 147:432–40
    [Google Scholar]
  93. 93.  Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pévet M et al. 2008. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr. Biol. 18:1147–52
    [Google Scholar]
  94. 94.  Jansen HT, Cutter C, Hardy S, Lehman MN, Goodman RL 2003. Seasonal plasticity within the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in identified GnRH inputs and glial association. Endocrinology 144:3663–76
    [Google Scholar]
  95. 95.  Anderson GM, Hardy SL, Valent M, Billings HJ, Connors JM, Goodman RL 2003. Evidence that thyroid hormones act in the ventromedial preoptic area and the premammillary region of the brain to allow the termination of the breeding season in the ewe. Endocrinology 144:2892–901
    [Google Scholar]
  96. 96.  Billings HJ, Viguié C, Karsch FJ, Goodman RL, Connors JM, Anderson GM 2002. Temporal requirements of thyroid hormones for seasonal changes in luteinizing hormone secretion. Endocrinology 143:2618–25
    [Google Scholar]
  97. 97.  Schuster C, Gauer F, Guerrero H, Lakhdar-Ghazal N, Pévet P, Masson-Pévet M 2000. Photic regulation of mt1 melatonin receptors in the Siberian hamster pars tuberalis and suprachiasmatic nuclei: involvement of the circadian clock and intergeniculate leaflet. J. Neuroendocrinol. 12:207–16
    [Google Scholar]
  98. 98.  Song CK, Bartness TJ 2001. CNS sympathetic outflow neurons to white fat that express MEL receptors may mediate seasonal adiposity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R666–72
    [Google Scholar]
  99. 99.  Klosen P, Bienvenu C, Demarteau O, Dardente H, Guerrero H et al. 2002. The mt1 melatonin receptor and RORb receptor are co-localized in specific TSH-immunoreactive cells in the pars tuberalis of the rat pituitary. J. Histochem. Cytochem. 50:1647–57
    [Google Scholar]
  100. 100.  Wittkowski W, Bergmann M, Hoffmann K, Pera F 1988. Photoperiod-dependent changes in TSH-like immunoreactivity of cells in the hypophysial pars tuberalis of the Djungarian hamster. Phodopus sungorus. Cell Tissue Res. 251:183–87
    [Google Scholar]
  101. 101.  Ebihara S, Marks T, Hudson DJ, Menaker M 1986. Genetic control of melatonin synthesis in the pineal gland of the mouse. Science 231:491–93
    [Google Scholar]
  102. 102.  Yasuo S, Yoshimura T, Ebihara S, Korf HW 2009. Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J. Neurosci. 29:2885–89
    [Google Scholar]
  103. 103.  Bockmann J, Böckers TM, Winter C, Wittkowski W, Winterhoff H et al. 1997. Thyrotropin expression in hypophyseal pars tuberalis-specific cells is 3,5,3′-triiodothyronine, thyrotropin-releasing hormone, and pit-1 independent. Endocrinology 138:1019–28
    [Google Scholar]
  104. 104.  Yamada M, Saga Y, Shibusawa N, Hirato J, Murakami M et al. 1997. Tertiary hypothyroidism and hyperglycemia in mice with targeted disruption of the thyrotropin-releasing hormone gene. PNAS 94:10862–67
    [Google Scholar]
  105. 105.  Ikegami K, Liao XH, Hoshino Y, Ono H, Ota W et al. 2014. Tissue-specific posttranslational modification allows functional targeting of thyrotropin. Cell Rep 9:801–10
    [Google Scholar]
  106. 106.  Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H 2010. Discovery and evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J. Neuroendocrinol. 22:716–27
    [Google Scholar]
  107. 107.  Revel FG, Saboureau M, Masson-Pévet M, Pévet P, Mikkelsen JD, Simonneaux V 2006. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr. Biol. 16:1730–35
    [Google Scholar]
  108. 108.  Ansel L, Bolborea M, Bentsen AH, Klosen P, Mikkelsen JD, Simonneaux V 2010. Differential regulation of Kiss1 expression by melatonin and gonadal hormones in male and female Syrian hamsters. J. Biol. Rhythms 25:81–91
    [Google Scholar]
  109. 109.  Ansel L, Bentsen AH, Ancel C, Bolborea M, Klosen P et al. 2011. Peripheral kisspeptin reverses short photoperiod-induced gonadal regression in Syrian hamsters by promoting GNRH release. Reproduction 142:417–25
    [Google Scholar]
  110. 110.  Tsutsui K, Ubuka T, Bentley GE, Kriegsfeld LJ 2013. Review: regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front. Neurosci. 7:60
    [Google Scholar]
  111. 111.  Clarke IJ, Sari IP, Qi Y, Smith JT, Parkington HC et al. 2008. Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 149:5811–21
    [Google Scholar]
  112. 112.  Ancel C, Bentsen AH, Sébert ME, Tena-Sempere M, Mikkelsen JD, Simonneaux V 2012. Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male Syrian hamster: The exception proves the rule. Endocrinology 153:1352–63
    [Google Scholar]
  113. 113.  Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K et al. 2012. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 153:373–85
    [Google Scholar]
  114. 114.  Simonneaux V, Ancel C, Poirel VJ, Gauer F 2013. Kisspeptins and RFRP-3 act in concert to synchronize rodent reproduction with seasons. Front. Neurosci. 7:22
    [Google Scholar]
  115. 115.  Cyr DG, Bromage NR, Duston J, Eales JG 1988. 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. 69:217–25
    [Google Scholar]
  116. 116.  Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K et al. 2013. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat. Commun. 4:2108
    [Google Scholar]
  117. 117.  Borg B 2010. Photoperiodism in fishes. Photoperiodism: The Biological Calendar RJ Nelson, DL Denlinger, DE Somers 371–98 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  118. 118.  Takahashi JS, Hamm H, Menaker M 1980. Circadian rhythms of melatonin release from individual superfused chicken pineal glands in vitro. PNAS 77:2319–22
    [Google Scholar]
  119. 119.  Menaker M, Wisner S 1983. Temperature-compensated circadian clock in the pineal of Anolis. . PNAS 80:6119–21
    [Google Scholar]
  120. 120.  Maeda R, Shimo T, Nakane Y, Nakao N, Yoshimura T 2015. Ontogeny of the saccus vasculosus, a seasonal sensor in fish. Endocrinology 156:4238–43
    [Google Scholar]
  121. 121.  Shimmura T, Nakayama T, Shinomiya A, Fukamachi S, Yasugi M et al. 2017. Dynamic plasticity in phototransduction regulates seasonal changes in color perception. Nat. Commun. 8:412
    [Google Scholar]
  122. 122.  Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE 1995. A behavioral screen for isolating zebrafish mutants with visual system defects. PNAS 92:10545–49
    [Google Scholar]
  123. 123.  Fu Y, Yau KW 2007. Phototransduction in mouse rods and cones. Pflügers Arch 454:805–19
    [Google Scholar]
  124. 124.  Parker RO, Crouch RK 2010. Retinol dehydrogenases (RDHs) in the visual cycle. Exp. Eye Res. 91:788–92
    [Google Scholar]
  125. 125.  Niwa-Suzuki H 1965. Effects of castration and administration of methyl testosterone on the nuptial coloration of the medaka (Oryzias latipes). Embryologia 8:289–98
    [Google Scholar]
  126. 126.  Matsumoto Y, Fukamachi S, Mitani H, Kawamura S 2006. Functional characterization of visual opsin repertoire in medaka (Oryzias latipes). Gene 371:268–78
    [Google Scholar]
  127. 127.  Ikegami K, Katou Y, Higashi K, Yoshimura T 2009. Localization of circadian clock protein BMAL1 in the photoperiodic signal transduction machinery in Japanese quail. J. Comp. Neurol. 517:397–404
    [Google Scholar]
  128. 128.  Yasuo S, Watanabe M, Okabayashi N, Ebihara S, Yoshimura T 2003. 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 144:3742–48
    [Google Scholar]
  129. 129.  Dardente H, Menet JS, Poirel VJ, Streicher D, Gauer F et al. 2003. Melatonin induces Cry1 expression in the pars tuberalis of the rat. Brain Res. Mol. Brain Res. 114:101–6
    [Google Scholar]
  130. 130.  Johnston JD, Ebling FJ, Hazlerigg DG 2005. Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur. J. Neurosci. 21:2967–74
    [Google Scholar]
  131. 131.  Lincoln G, Messager S, Andersson H, Hazlerigg DG 2002. Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. PNAS 99:13890–95
    [Google Scholar]
  132. 132.  Messager S, Ross AW, Barrett P, Morgan PJ 1999. Decoding photoperiodic time through Per1 and ICER gene amplitude. PNAS 96:9938–43
    [Google Scholar]
  133. 133.  Yasuo S, Watanabe M, Tsukada A, Takagi T, Iigo M et al. 2004. Photoinducible phase-specific light induction of Cry1 gene in the pars tuberalis of Japanese quail. Endocrinology 145:1612–16
    [Google Scholar]
  134. 134.  Lincoln G, Andersson H, Loudon A 2003. Clock genes in calendar cells as the basis of annual timekeeping in mammals—a unifying hypothesis. J. Endocrinol. 179:1–13
    [Google Scholar]
  135. 135.  Dardente H, Wyse C, Birnie M, Dupré S, Loudon A et al. 2010. A molecular switch for photoperiod responsiveness in mammals. Curr. Biol. 20:2193–98
    [Google Scholar]
  136. 136.  Masumoto K, Ukai-Tadenuma M, Kasukawa T, Nagano M, Uno KD et al. 2010. Acute induction of Eya3 by late-night light stimulation triggers TSHβ expression in photoperiodism. Curr. Biol. 20:2199–206
    [Google Scholar]
  137. 137.  Sawara Y, Egami N 1977. Note on the differences in the response of the gonad to photoperiod among populations of Oryzias latipes collected in different localities. Annot. Zool. Jpn. 50:147–50
    [Google Scholar]
  138. 138.  Kasahara T, Abe K, Mekada K, Yoshiki A, Kato T 2010. Genetic variation of melatonin productivity in laboratory mice under domestication. PNAS 107:6412–17
    [Google Scholar]
  139. 139.  Shimomura K, Lowrey PL, Vitaterna MH, Buhr ED, Kumar V et al. 2010. Genetic suppression of the circadian clock mutation by the melatonin biosynthesis pathway. PNAS 107:8399–403
    [Google Scholar]
  140. 140.  Rubin CJ, Zody MC, Eriksson J, Meadows JR, Sherwood E et al. 2010. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464:587–91
    [Google Scholar]
  141. 141.  Stevenson TJ, Visser ME, Arnold W, Barrett P, Biello S et al. 2015. Disrupted seasonal biology impacts health, food security and ecosystems. Proc. Biol. Sci. 282:1453
    [Google Scholar]
  142. 142.  Wirz-Justice A 2017. Seasonality in affective disorders. Gen. Comp. Endocrinol. 258:244–49
    [Google Scholar]
  143. 143.  Carney PA, Fitzgerald CT, Monaghan CE 1988. Influence of climate on the prevalence of mania. Br. J. Psychiatry 152:820–23
    [Google Scholar]
  144. 144.  Maes M, Meltzer HY, Suy E, De Meyer F 1993. Seasonality in severity of depression: relationships to suicide and homicide occurrence. Acta Psychiatr. Scand. 88:156–61
    [Google Scholar]
  145. 145.  Parker G, Walter S 1982. Seasonal variation in depressive disorders and suicidal deaths in New South Wales. Br. J. Psychiatry 140:626–32
    [Google Scholar]
  146. 146.  Rosenthal NE, Sack DA, Gillin JC, Lewy AJ, Goodwin FK et al. 1984. Seasonal affective disorder: a description of the syndrome and preliminary findings with light therapy. Arch. Gen. Psychiatry 41:72–80
    [Google Scholar]
  147. 147.  Hirota T, Lee JW, St. John PC, Sawa M, Iwaisako K et al. 2012. Identification of small molecule activators of cryptochrome. Science 337:1094–97
    [Google Scholar]
  148. 148.  Oshima T, Yamanaka I, Kumar A, Yamaguchi J, Nishiwaki-Ohkawa T et al. 2015. C-H activation generates period-shortening molecules that target cryptochrome in the mammalian circadian clock. Angew. Chem. Int. Ed. 54:7193–97
    [Google Scholar]
  149. 149.  Tamai TK, Nakane Y, Ota W, Kobayashi A, Ishiguro M et al. 2018. Identification of circadian clock modulators from existing drugs. EMBO Med. Mol. 10:e8724
    [Google Scholar]
  150. 150.  Nakane Y, Yoshimura T 2014. Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates. Front. Neurosci. 8:115
    [Google Scholar]
/content/journals/10.1146/annurev-animal-020518-115216
Loading
/content/journals/10.1146/annurev-animal-020518-115216
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error