Regulation of seasonal reproduction by hypothalamic activation of thyroid hormone

Frontiers in Endocrinology

Volumn 5, Issue FEB, 2014, Pages

  Shinomiya, Ai ^a   Shimmura, Tsuyoshi ^a,b   Nishiwaki Ohkawa, Taeko ^b   Yoshimura, Takashi ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Ependymal cell; Iodothyronine deiodinase; Mediobasal hypothalamus; Pars tuberalis; Seasonal reproduction; Thyroid hormone; Thyrotropin

Indexed keywords

ACETYLSEROTONIN METHYLTRANSFERASE; ARALKYLAMINE ACETYLTRANSFERASE; DEIODINASE; ENZYME; EYES ABSENT 3; GONADOTROPIN; LIOTHYRONINE; MELANOPSIN; MELATONIN; MELATONIN RECEPTOR; MONOCARBOXYLATE TRANSPORTER 8; NEUROPSIN; OPSIN; ORGANIC ANION TRANSPORTER F; PEPTIDES AND PROTEINS; RHODOPSIN; THYROID HORMONE; THYROID HORMONE RECEPTOR; THYROTROPIN; THYROTROPIN RECEPTOR; THYROXINE; UNCLASSIFIED DRUG;

DOMESTICATION; ENZYME REGULATION; EPENDYMA CELL; GENE EXPRESSION; HYPOTHALAMUS; MEDIOBASAL HYPOTHALAMUS; NONHUMAN; PHOTOPERIODICITY; REPRODUCTION; REVIEW; SEASONAL REPRODUCTION; SEASONAL VARIATION; SIGNAL TRANSDUCTION; THYROIDECTOMY;

EID: 84901061399     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00012     Document Type: Review

References (93)

1. 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.
2. Dawson A, King VM, Bentley GE, Ball GF. Photoperiodic control of seasonality in birds. J Biol Rhythms (2001) 16:365-80. doi:10.1177/074873001129002079.
3. 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.
4. Hahn TP, MacDougall-Shackleton SA. Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos Trans R Soc Lond B Biol Sci (2008) 363:267-86. doi:10.1098/rstb.2007.2139.
5. Nicholls TJ, Goldsmith AR, Dawson A. Photorefractoriness in birds and comparison with mammals. Physiol Rev (1988) 68:133-76.
6. Cyr DG, Eales JG. Interrelationships between thyroidal and reproductive endocrine systems in fish. Rev Fish Biol Fish (1996) 6:165-200. doi:10.1007/BF00182342.
7. Nicholls TJ, Follett BK, Goldsmith AR, Pearson H. Possible homologies between photorefractoriness in sheep and birds: the effect of thyroidectomy on the length of the ewe's breeding season. Reprod Nutr Dev (1988) 28:375-85. doi:10.1051/rnd:19880304.
8. Moenter SM, Woodfill CJ, Karsch FJ. Role of the thyroid gland in seasonal reproduction: thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes. Endocrinology (1991) 128:1337-44. doi:10.1210/endo-128-3-1337.
9. Dawson A. Thyroidectomy progressively renders the reproductive system of starlings (Sturnus vulgaris) unresponsive to changes in daylength. J Endocrinol (1993) 139:51-5. doi:10.1677/joe.0.1390051.
10. Dawson A. Thyroidectomy of house sparrows (Passer domesticus) prevents photo-induced testicular growth but not the increased hypothalamic gonadotrophin-releasing hormone. Gen Comp Endocrinol (1998) 110:196-200. doi:10.1006/gcen.1998.7065.
11. Parkinson TJ, Follett BK. Thyroidectomy abolishes seasonal testicular cycles of Soay rams. Proc Biol Sci (1995) 259:1-6. doi:10.1098/rspb.1995.0001.
12. Follett BK, Nicholls TJ. Influences of thyroidectomy and thyroxine replacement on photoperiodically controlled reproduction in quail. J Endocrinol (1985) 107:211-21. doi:10.1677/joe.0.1070211.
13. Goldsmiths AR, Nicholls TJ. Thyroxine effects upon reproduction, prolactin secretion and plumage moult in thyroidectomised European starlings Sturnus vulgaris. Ornis Scand (1992) 23:398-404. doi:10.2307/3676666.
14. Wilson FE, Reinert BD. Thyroid hormone acts centrally to programme photostimulated male American tree sparrows (Spizella arborea) for vernal and autumnal components of seasonality. J Neuroendocrinol (2000) 12:87-95. doi:10.1046/j.1365-2826.2000.00437.x.
15. Bentley GE. Photoperiodism and reproduction in birds. In: Nelson RJ, Denlinger DL, Somers DE editors. Photoperiodism: The Biological Calendar. New York: Oxford University Press (2010). p. 420-45.
16. 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.
17. Sharp PJ, Follett BK. The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology (1969) 5:205-18. doi:10.1159/000121861.
18. 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. doi:10.1098/rspb.1993.0121.
19. Meddle SL, Follett BK. Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neuroscience (1997) 17:8909-18.
20. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, et al. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature (2003) 426:178-81. doi:10.1038/nature02117.
21. Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK, Ebihara S, et al. 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. doi:10.1210/en.2005-0057.
22. Bernal J. Action of thyroid hormone in brain. J Endocrinol Invest (2002) 25:268-88.
23. Watanabe T, Yamamura T, Watanabe M, Yasuo S, Nakao N, Dawson A, et al. 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. doi:10.1152/ajpregu.00521.2006.
24. Ono H, Nakao N, Yamamura T, Kinoshita K, Mizutani M, Namikawa T, et al. Red jungle fowl (Gallus gallus) as a model for studying the molecular mechanism of seasonal reproduction. Anim Sci J (2009) 80:328-32. doi:10.1111/j.1740-0929.2009.00628.x.
25. 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. doi:10.1371/journal.pone.0034997.
26. 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. doi:10.1111/j.1460-9568.2012.08209.x.
27. Barrett P, Ebling FJ, Schuhler S, Wilson D, Ross AW, Warner A, et al. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology (2007) 148:3608-17. doi:10.1210/en.2007-0316.
28. Freeman DA, Teubner BJ, Smith CD, Prendergast BJ. Exogenous T3 mimics long day lengths in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol (2007) 292:R2368-72. doi:10.1152/ajpregu.00713.2006.
29. Herwig A, Wilson D, Logie TJ, Boelen A, Morgan PJ, Mercer JG, et al. 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 (2009) 296:R1307-15. doi:10.1152/ajpregu.90755.2008.
30. Watanabe M, Yasuo S, Watanabe T, Yamamura T, Nakao N, Ebihara S, et al. Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology (2004) 145:1546-9. doi:10.1210/en.2003-1593.
31. Revel FG, Saboureau M, Pévet P, Mikkelsen JD, Simonneaux V. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology (2006) 147:4680-7. doi:10.1210/en.2006-0606.
32. Yasuo S, Yoshimura T, Ebihara S, Korf HW. Temporal dynamics of type 2 deiodinase expression after melatonin injections in Syrian hamsters. Endocrinology (2007) 148:4385-92. doi:10.1210/en.2007-0497.
33. Ross AW, Helfer G, Russell L, Darras VM, Morgan PJ. Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of F344 rats. PLoS One (2011) 6:e21351. doi:10.1371/journal.pone.0021351.
34. Yasuo S, Watanabe M, Iigo M, Nakamura TJ, Watanabe T, Takagi T, et al. 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 (2007) 292:R1315-9. doi:10.1152/ajpregu.00396.2006.
35. Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, et al. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci USA (2008) 105:18238-42. doi:10.1073/pnas.0808952105.
36. Yasuo S, Nakao N, Ohkura S, Iigo M, Hagiwara S, Goto A, et al. 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 (2006) 147:432-40. doi:10.1210/en.2005-0507.
37. Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pévet M, Morgan PJ, et al. Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol (2008) 18:1147-52. doi:10.1016/j.cub.2008.06.076.
38. Anderson GM, Hardy SL, Valent M, Billings HJ, Connors JM, Goodman RL. 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 (2003) 144:2892-901. doi:10.1210/en.2003-0322.
39. Billings HJ, Viguié C, Karsch FJ, Goodman RL, Connors JM, Anderson GM. Temporal requirements of thyroid hormones for seasonal changes in luteinizing hormone secretion. Endocrinology (2002) 143:2618-25. doi:10.1210/en.143.7.2618.
40. Ikegami K, Yoshimura T. Circadian clocks and the measurement of daylength in seasonal reproduction. Mol Cell Endocrinol (2012) 349:76-81. doi:10.1016/j.mce.2011.06.040.
41. Abe T, Suzuki T, Unno M, Tokui T, Ito S. Thyroid hormone transporters: recent advances. Trends Endocrinol Metab (2002) 13:215-20. doi:10.1016/S1043-2760(02)00599-4.
42. 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. Pflugers Arch (2004) 447:653-65. doi:10.1007/s00424-003-1168-y.
43. Nakao N, Takagi T, Iigo M, Tsukamoto T, Yasuo S, Masuda T, et al. Possible involvement of organic anion transporting polypeptide 1c1 in the photoperiodic response of gonads in birds. Endocrinology (2006) 147:1067-73. doi:10.1210/en.2005-1090.
44. 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. doi:10.1677/joe.0.0970121.
45. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, et al. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature (2008) 452:317-22. doi:10.1038/nature06738.
46. Benoit J. Le role des yeux dans l'action stimulante de la lumiere sure le developpement testiulaire chez le canard. C R Soc Biol (Paris) (1935) 118:669-71.
47. Oliver J, Bayle JD. Brain photoreceptors for the photoinduced testicular response in birds. Experientia (1982) 38:1020-9. doi:10.1007/BF01955346.
48. Max M, McKinnon PJ, Seidenman KJ, Barrett RK, Applebury ML, Takahashi JS, et al. Pineal opsin: a nonvisual opsin expressed in chick pineal. Science (1995) 267:1502-6. doi:10.1126/science.7878470.
49. Okano T, Yoshizawa T, Fukada Y. Pinopsin is a chicken pineal photoreceptive molecule. Nature (1994) 372:94-7. doi:10.1038/372094a0.
50. Siopes TD, Wilson WO. Extraocular modification of photoreception in intact and pinealectomized coturnix. Poult Sci (1974) 53:2035-41. doi:10.3382/ps.0532035.
51. 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 USA (1970) 67:320-5. doi:10.1073/pnas.67.1.320.
52. 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. doi:10.1007/BF00221754.
53. Wada Y, Okano T, Adachi A, Ebihara S, Fukada Y. Identification of rhodopsin in the pigeon deep brain. FEBS Lett (1998) 424:53-6. doi:10.1016/S0014-5793(98)00138-0.
54. Bailey MJ, Cassone VM. Melanopsin expression in the chick retina and pineal gland. Brain Res Mol Brain Res (2005) 134:345-8. doi:10.1016/j.molbrainres.2004.11.003.
55. Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, et al. 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. doi:10.1111/j.1471-4159.2004.02874.x.
56. 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. doi:10.1016/j.neuroscience.2010.06.082.
57. 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. doi:10.1002/dvdy.20600.
58. 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. doi:10.1016/j.modgep.2007.06.001.
59. Davies WI, Turton M, Peirson SN, Follett BK, Halford S, Garcia-Fernandez JM, et al. Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol Lett (2012) 8:291-4. doi:10.1098/rsbl.2011.0864.
60. Halford S, Pires SS, Turton M, Zheng L, Gonzalez-Menendez I, Davies WL, et al. VA opsin-based photoreceptors in the hypothalamus of birds. Curr Biol (2009) 19:1396-402. doi:10.1016/j.cub.2009.06.066.
61. Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, et al. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci USA (2010) 107:15264-8. doi:10.1073/pnas.1006393107.
62. 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 USA (2010) 107:22084-9. doi:10.1073/pnas.1012498107.
63. Groos GA, van der Kooy D. Functional absence of brain photoreceptors mediating entrainment of circadian rhythms in the adult rat. Experientia (1981) 37:71-2. doi:10.1007/BF01965576.
64. Legan SJ, Karsch FJ. Importance of retinal photoreceptors to the photoperiodic control of seasonal breeding in the ewe. Biol Reprod (1983) 29:316-25. doi:10.1095/biolreprod29.2.316.
65. Lockley SW, Skene DJ, Thapan K, English J, Ribeiro D, Haimov I, et al. Extraocular light exposure does not suppress plasma melatonin in humans. J Clin Endocrinol Metab (1998) 83:3369-72. doi:10.1210/jc.83.9.3369.
66. Meijer JH, Thio B, Albus H, Schaap J, Ruijs ACJ. Functional absence of extraocular photoreception in hamster circadian rhythms entrainment. Brain Res (1999) 831:337-9. doi:10.1016/S0006-8993(99)01509-7.
67. Nelson RJ, Zucker I. Absence of extraocular photoreception in diurnal and nocturnal rodents exposed to direct sunlight. Comp Biochem Physiol (1981) 69A:145-8. doi:10.1016/0300-9629(81)90651-4.
68. Reiter RJ. The pineal and its hormones in the control of reproduction in mammals. Endocr Rev (1980) 1:109-31. doi:10.1210/edrv-1-2-109.
69. Yamazaki S, Goto M, Menaker M. No evidence for extraocular photoreceptors in the circadian system of the Syrian hamster. J Biol Rhythms (1999) 14:197-201. doi:10.1177/074873099129000605.
70. Inouye ST, Kawamura H. Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA (1979) 76:5962-6. doi:10.1073/pnas.76.11.5962.
71. Klein DC, Moore RY, Reppert SM. Suprachiasmatic Nucleus: The Mind's Clock. New York: Oxford University Press (1991).
72. Lehman MN, Silver R, Gradstone WR, Kahn RM, Gibson M, Bittman EL. Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J Neurosci (1987) 7:1626-38.
73. Ralph MR, Foster RG, Davis FC, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science (1990) 247:975-8. doi:10.1126/science.2305266.
74. Arendt J. Melatonin and the Mammalian Pineal Gland. London: Chapman & Hall (1995).
75. Hoffman RA, Reiter RJ. Pineal gland: influence on gonads of male hamsters. Science (1965) 148:1609-11. doi:10.1126/science.148.3677.1609.
76. Reppert SM, Weaver DR, Ebisawa T. Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses. Neuron (1994) 13:1177-85. doi:10.1016/0896-6273(94)90055-8.
77. Reppert SM, Godson CG, Mahle CD, Weaver DR, Slaugenhaupt SA, Gusella JF. Molecular characterization of a second melatonin receptor expressed in human retina and brain: the Mel1b-melatonin receptor. Proc Natl Acad Sci USA (1995) 92:8734-8. doi:10.1073/pnas.92.19.8734.
78. Schuster C, Gauer F, Guerrero H, Lakhdar-Ghazal N, Pévet P, Masson-Pévet M. 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 (2000) 12:207-16. doi:10.1046/j.1365-2826.2000.00039.x.
79. Song CK, Bartness TJ. CNS sympathetic outflow neurons to white fat that express MEL receptors may mediate seasonal adiposity. Am J Physiol Regul Integr Comp Physiol (2001) 281:R666-72.
80. Klosen P, Bienvenu C, Demarteau O, Dardente H, Guerrero H, Pévet P, et al. 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 (2002) 50:1647-57. doi:10.1177/002215540205001209.
81. Wittkowski W, Bergmann M, Hoffmann K, Pera F. Photoperiod-dependent changes in TSH-like immunoreactivity of cells in the hypophysial pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res (1988) 251:183-7. doi:10.1007/BF00215463.
82. Ebihara S, Marks T, Hudson DJ, Menaker M. Genetic control of melatonin synthesis in the pineal gland of the mouse. Science (1986) 231:491-3. doi:10.1126/science.3941912.
83. Goto M, Oshima I, Tomita T, Ebihara S. Melatonin content of the pineal gland in different mouse strains. J Pineal Res (1989) 7:195-204. doi:10.1111/j.1600-079X.1989.tb00667.x.
84. Yasuo S, Yoshimura T, Ebihara S, Kolf HW. Melatonin transmits photoperiodic signals through the MT1 melatonin receptor. J Neurosci (2009) 29:2885-9. doi:10.1523/JNEUROSCI.0145-09.2009.
85. 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. doi:10.1210/en.2004-0366.
86. Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, et al. 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. doi:10.1016/S0306-4522(99)00383-8.
87. 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. doi:10.1007/s00441-005-0126-8.
88. Jansen HT, Cutter C, Hardy S, Lehman MN, Goodman RL. Seasonal plasticity within the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in identified GnRH inputs and glial association. Endocrinology (2003) 144:3663-76. doi:10.1210/en.2002-0188.
89. Yoshimura T. Molecular bases for seasonal reproduction in birds. J Poult Sci (2004) 41:251-8. doi:10.1016/j.yfrne.2013.10.002.
90. Kasahara T, Abe K, Mekada K, Yoshiki A, Kato T. Genetic variation of melatonin productivity in laboratory mice under domestication. Proc Natl Acad Sci USA (2010) 107:6412-7. doi:10.1073/pnas.0914399107.
91. Shimomura K, Lowrey PL, Vitaterna MH, Buhr ED, Kumar V, Hanna P, et al. Genetic suppression of the circadian clock mutation by the melatonin biosynthesis pathway. Proc Natl Acad Sci USA (2010) 107:8399-403. doi:10.1073/pnas.1004368107.
92. Rubin CJ, Zody MC, Eriksson J, Meadows JR, Sherwood E, Webster MT, et al. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature (2010) 464:587-91. doi:10.1038/nature08832.
93. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, et al. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun (2013) 4:2108. doi:10.1038/ncomms3108.