Summary
The direction of change in daylength provides the seasonal time cue for the timing of puberty in many mammalian species. The pattern of melatonin secretion from the pineal gland transduces the environmental light-dark cycle into a signal influencing the neuroendocrine control of sexual maturation. The change in duration of nocturnal melatonin secretion is probably the key feature of the melatonin signal which conveys daylength information. This information may also be used by neuroendocrine axes controlling seasonal changes in pelage colour, growth and metabolism. The mechanism of action of melatonin on neuroendocrine pathways is unknow. Although the ability to synthesize and secrete melatonin in a pattern that reflects the duration of the night may not occur until the postnatal period, the rodent and ovine foetus has the ability to respond in utero to photoperiodic cues to which its mother is exposed in late gestation. Transplacental passage of maternal melatonin is likely to be the mechanism by which photoperiodic cues reach the foetus. Species which do not exhibit seasonal patterns of puberty, such as the human, also secrete melatonin in a pattern which reflects the environmental light-dark cycle, but they do not respond reproductively to the seasonal melatonin information.
Similar content being viewed by others
Literature
Attanasio, A., Rager, K., and Gupta, D., Ontogeny of circadian rhythmicity for melatonin, serotonin and N-acetylserotonin in human. J. Pineal Res.3 (1986) 251–256.
Bartness, T. J. and Goldman, B. D., Peak duration of serum melatonin and short-day responses in adult Siberian hamsters. Am. J. Physiol.255 (1988) R812-R822.
Bartness, T. J. and Goldman, B. D., Effects of melatonin on long-day responses in short-day housed adult Siberian hamsters. Am. J. Physiol.255 (1988) R823-R830.
Bartness, T. J. and Goldman, B. D., Mammalian pineal melatonin: A clock for all seasons. Experientia45 (1989) 939–945.
Bassett, J. M., Bomford, J., and Mott, J., Photoperiod: an important regulator of plasma prolactin concentration in fetal lambs during late gestation. Quart. J. exp. Physiol.73 (1988) 241–244.
Boyd, I. L., The effect of photoperiod and melatonin on testis development and regression in wild European rabbits (Oryctolagus cuniculus). Biol. Reprod.33 (1985) 21–29.
Brackmann, M., and Hoffman, K. Pinealectomy and photoperiod influence testicular development in the Djungarian hamster. Naturwissenschaften64 (1977) 341–342.
Bronson, F. H., and Rissman, E. F., The biology of puberty. Biol. Rev.61 (1986) 157–195.
Brown, B., and Forbes, J. M., Diurnal variations of plasma prolactin in growing sheep under two lighting regimes and the effect of pinealectomy. J. Endocr.84 (1980) 91–99.
Cameron, J. L., Hansen, P. D., McNeill, T. M., Koerker, D. J., Clifton, D. K., Rogers, K. V., Bremner, W. S., and Steiner, R. A., Metabolic cues for the onset of puberty in primate species, in: Adolescence in Females, p. 59–78. Eds, C. Flamigni, S. Venturoli and J. R. Givens, Year Book Medical Publishers, Chicago 1985.
Carter, D. S., and Goldman, B. D., Antigonadal, effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungoris sungoris): duration is the critical parameter. Endocrinology113 (1983) 1261–1267.
Carter, D. S., and Goldman, B. D., Progonadal role of the pineal in the Djungarian hamster: mediation by melatonin. Endocrinology113 (1983) 1268–1273.
Charlton, H. M., Grocock, C. A. and Ostberg, A., The effects of pinealectomy and superior cervical ganglionectomy on the testis of the vole,Microtus agrestis. J. Reprod. Fert.48 (1976) 377–379.
Claypool, L. E., Wood, R. I., Yellon, S. M., and Foster, D. L., The ontogeny of melatonin secretion in the lamb. Endocrinology (in press).
Darrow, J. M., Davis F. C., Elliott, J. A., Stetson, M. H., Turek, F. W., and Menaker, M., Influence of photoperiod on reproductive development in the golden hamster. Biol. Reprod.22 (1980) 443–450.
Darrow, J. M., and Goldman, B. D., Circadian regulation of pineal melatonin and reproduction in the Djungarian hamster. J. biol. Rhythms1 (1986) 39–54.
Day, M. L., Imakawa, K., Zalesky, D. D., Kittok, R. J., and Kinder, J. E., Effects of restriction of dietary energy intake during the prepubertal period on secretion of luteinizing hormone and responsiveness of the pituitary to luteinizing hormone-releasing hormone in heifers. J. Anim. Sci.62 (1986) 1641–1648.
Dubocovich, M. L., Pharmacology and function of melatonin receptors. FASEB J.2 (1988) 2765–2773.
Ducker, M. J., Bowman, J. C., and Temple, A., The effect of constant photoperiod on the expression of oestrus in the ewe. J. Reprod. Fert. Suppl.19 (1973) 143–150.
Ebling, F. J. P., and Foster, D. L., Photoperiod requirements for puberty differ from those for onset of the adult breeding season in sheep. J. Reprod. Fert.84 (1988) 283–293.
Ebling, F. J. P., and Lincoln, G. A., β-Endorphin secretion in rams related to season and photoperiod. Endocrinology120 (1987) 809–818.
Ebling, F. J. P., Claypool, L. E., and Foster, D. L., Neuroendocrine responsiveness to light during the neonatal period in the sheep. J. Endocr.119 (1988) 211–218.
Ebling, F. J. P., Wood, R. I., Suttie, J. M., Adel, T. E., and Foster, D. L., Prenatal photoperiod influences neonatal prolactin secretion in the sheep. Endocrinology125 (1989) 384–391.
Ehrenkrantz, J. R. L., Tamarkin, L., Comite, F., Johnsonbaugh, R. E., Bybee, D. E., Loriaux, D. L., and Cutler, G. B., Daily rhythm of plasma melatonin in normal and precocious puberty. J. clin. Endocr. Metab.55 (1982) 307–310.
Eisemann, J. H., Bauman, D. E., Hogue, D. E., and Travis, H. F., Influence of photoperiod and prolactin on body composition and in vitro lipid metabolism in wether lambs. J. Anim. Sci.59 (1984) 95–104.
Fevre, M., Segel, T., Marks, J. M., and Boyar, R. M., LH and melatonin secretion patterns in pubertal boys. J. clin. Endocr. Metab.47 (1979) 1383–1386.
Follett, B. K., Photoperiodism and seasonal breeding in birds and mammals, in: Control of Ovulation, p. 267–293. Eds D. B. Creighton, G. R. Foxcroft, N. B. Haynes, and G. E. Lamming. Butterworths, London 1978.
Forbes, J. M., Driver, P. M., Brown, W. B., Scanes, C. G., and Hart, I. C.. The effect of daylength on the growth of lambs. 2. Blood concentrations of growth hormone, prolactin, insulin and thyroxine, and the effect of feeding. Anim. Prod.29 (1979) 43.
Foster, D. L., Comparative development of mammalian females: proposed analogies among patterns of LH secretion in various species, in: Problems in Pediatric Endocrinology, p. 193–210. Eds C. La Cauza and A. W. Root. Academic Press, London 1980.
Foster, D. L., Mechanism for delay of first ovulation in lambs born in the wrong season (fall). Biol. Reprod.25 (1981) 85–92.
Foster, D. L., and Olster, D. H., Effect of restricted nutrition on puberty in the lamb: patterns of tonic luteinizing hormone (LH) secretion and competency of the LH surge system. Endocrinology116 (1985) 375–381.
Foster, D. L., Ebling, F. J. P., and Claypool, L. E., Timing of puberty by photoperiod. Reprod. Nutr. Develop.28 (1988) 349–364.
Foster, D. L., Ebling, F. J. P., Claypool, L. E., and Woodfill, C. J. I., Cessation of long-day melatonin rhythms time, puberty in a shortday breeder. Endocrinology123 (1988) 1636–1641.
Foster, D. L., Karsch, F. J., Olster, D. H., Ryan, K. D., and Yellon, S. M., Determinants of puberty in a seasonal breeder. Rec. Prog. Horm. Res.42 (1986) 330–384.
Foster, D. L., Yellon, S. M., Ebling, F. J. P., and Claypool, L. E., Are ambient short-day cues necessary for puberty in a short-day breeder? Biol. Reprod.38 (1988) 821–829.
Goldman, B. D., The physiology of melatonin in mammals, in: Pineal Research Reviews, p. 145–182. Ed. R. J. Reiter, Alan R. Liss, New York 1983.
Goldman, B. D., and Darrow, J. M., The pineal gland and mammalian photoperiodism. Neuroendocrinology37 (1983) 386–396.
Goldman, B. D., Darrow, J. M., and Yogev, L., Effects of timed melatonin infusions on reproductive development in the Djungarian hamster (Phodopus sungorus). Endocrinology114 (1984) 2076–2083.
Gupta, D., Human development and the pineal gland in: The Pineal Gland During Development: From Fetus to Adult, p. 117–133. Eds D. Gupta and R. J. Reiter, Croom Helm, London 1986.
Hartmann, L., Roger, M., Lemaitre, B. J., Massias, J. F., and Chaussain, J. L., Plasma and urinary melatonin in male infants during the first 12 months of life. Clinica chim. Acta121 (1982), 37–42.
Hastings, M. H., Herbert, J., Hutchinson, J., Powers, J. B., Steel, E. A., and Walker, A. P., Differential neuroendocrine effects on photoperiodic history on the response of gonadotrophins and prolactin to intermediate day-lengths in the male Syrian hamster. J. biol. Rhythms (1989) in press.
Hoffman, K., Effect of short photoperiods on puberty, growth, and moult in the Djungarian hamster (Phodopus sungoris). J. Reprod. Fert.54 (1978) 29–35.
Hoffman, K., Illnerova, H., and Vanecek, J., Change in duration of the nighttime melatonin peak may be a signal driving photoperiodic responses in the Djungarian hamster. Neurosci. Lett.67 (1986) 68–72.
Horton, T. H., Cross-fostering of voles demonstrates in utero effects of photoperiod. Biol. Reprod.33 (1985) 934–939.
Horton, T. H., Growth and reproductive development of maleMicrotus montanus is affected by the prenatal photoperiod. Biol. Reprod.31 (1984) 499–504.
Karsch, F. J., Bittman, E. L., Foster, D. L., Goodman, R. L., Legan, S. J., and Robinson, J. E., Neuroendocrine basis of seasonal reproduction. Rec. Prog. Horm. Res.40 (1984) 185–232.
Kennaway, D. J., and Gilmore, T. A., Effects of melatonin implants in ewe lambs. J. Reprod. Fert.70 (1984) 39–45.
Kennaway, D. J., Gilmore, T. A., and Dunstan, E. A., Pinealectomy delays puberty in ewe lambs. J. Reprod. Fert.74 (1985) 119–125.
Kennedy, G. C., and Mitra, J., Body weight and food intake as initiating factors for puberty in the rat. J. Physiol.166 (1963) 408–418.
Klein, D. C., Evidence for the placental transfer of3H-acetyl-melatonin. Nature237 (1972) 117.
Lee, T. M., Smale, L., Zucker, I., and Dark, J., Influence of day-length experienced by dams on post-natal development of young meadow voles (Microtus pennsylvanicus). J. Reprod. Fert.81 (1987) 337–342.
Lee, T. M., and Zucker, I., Vole infant development is influenced perinatally by maternal photoperiodic history. Am. J. Physiol.255 (1988) R831-R838.
Lincoln, G. A., Light-induced rhythms of prolactin secretion in the ram and the effect of cranial sympathectomy. Acta endocr.91 (1979) 421–427.
Lincoln, G. A., and Ebling, F. J. P., Effect of constant-relase implants of melatonin on seasonal cycles in reproduction, prolactin secretion and moulting in rams. J. Reprod. Fert.73 (1985) 241–253.
Lincoln, G. A., McNeilly, A. S., and Cameron, C. L., The effects of a sudden decrease or increase in daylength on prolactin secretion in the ram. J. Reprod. Fert.52 (1978) 305–311.
McMillen, I. C., and Nowak, R., Maternal pinealectomy abolishes the diurnal rhythm in melatonin concentrations in the fetal sheep. J. Reprod. Fert. Abstract Ser.1 (1988) 19.
Moller, W., The human foetal pineal gland. Morphological indications of a photoreceptive capacity, in: The Pineal Gland During Development: From Fetus to Adult, p. 80–88. Eds, D. Gupta and R. J. Reiter, Croom Helm, London 1986.
Nowak, R., and Rodway, R. G., Effect of intravaginal implants of melation on the onset ovarian activity in adult and prepubertal ewes. J. Reprod. Fert.74 (1985) 287–293.
Oldham, C. M., and Gray, S. J., The ‘ram effect’ will advance puberty in 9 or 10 month old merino ewes independent of the season of birth. Proc. Aust. Soc. Anim. Prod.15 (1984) 727–728.
Plant, T. M., and Zorub, D. S., Pinealectomy in agonadal infantile male rhesus monkeys (Macaca mulatta) does not interrupt initiation of the prepubertal hiatus in gonadotropin secretion. Endocrinology118 (1986) 227–232.
Radford, H. M., Photoperiodism and sexual activity in Merino ewes. Aust. J. Agric. Res.12 (1960) 139–153.
Reiter, R. J., The pineal gland and pubertal development in mammals: a state of the art assessment, in, The Pineal Gland During Development: From Fetus to Adult, p. 100–116. Eds D. Gupta and R. J. Reiter. Croom Helm, London 1986.
Reppert, S. M., Chez, R. A., Anderson, A., and Klein, D. C., Maternal-fetal transfer of melatonin in the non-human primate. Pediatric Res.13 (1979) 788–791.
Rissman, E. F., Prepubertal sensitivity to melatonin in male hamsters. Biol. Reprod.22 (1980) 277–280.
Robinson, J. E., and Karsch, F. J., Photoperiodic history and a changing melatonin pattern can determine the neuroendocrine response of the ewe to daylength. J. Reprod. Fert.80 (1987) 159–165.
Rollag, M. D., and Stetson, M. H., Ontogeny of the pineal melatonin rhythm in golden hamsters. Biol. Reprod.24 (1981) 311.
Rollag, M. D., Dipinto, M. N., and Stetson, M. H., Ontogeny of the gonadal response of golden hamsters to short photoperiod, blinding, and melatonin. Biol. Reprod.27 (1982) 898–902.
Ryan, K. D., and Robinson, S. L., A rise in tonic luteinizing hormone secretion occurs during photoperiod-stimulated sexual maturation of the female ferret. Endocrinology116 (1985) 2013–2018.
Ryan, K. D., Maturation of ovarian function in female ferrets is influenced by photoperiod. J. Reprod. Fert.74 (1985) 503–507.
Silman, R. E., Leone, R. M., Hooper, R. J. L., and Preece, M. A., Melatonin, the pineal gland and human puberty. Nature282 (1979) 301–303.
Sisk, C. L., and Turek, F. W., Developmental time course of pubertal and photoperiodic changes in testosterone negative feedback on gonadotropin secretion in the golden hamster. Endocrinology112 (1983) 1208–1216.
Smith, A. J., Mondain-Monval, M., Andersen Berg, K., Simon, P., Forsberg, M., Clausen, O. P. F., Hansen, T., Moller, O. M., and Scholler, R., Effects of melatonin implantation on spermatogenesis, the moulting cycle and plasma concentrations of melatonin, LH, prolactin and testosterone in the male blue fox (Alopex lagopus). J. Reprod. Fert.79 (1987) 379–390.
Smith, I. D., The effect of constant long daily photoperiod upon the onset of puberty in ewes. J. agric. Sci.69 (1967) 43–45.
Sorrentino, S. Jr, Reiter, R. J., and Schalch, D. S., Interactions of the pineal gland, blinding, and underfeeding on reproductive organ size and radioimmunoassayable growth hormone. Neuroendocrinology7 (1971) 105–115.
Stansfield, S. C., Knight, P. G., Al-Mauly, N. Z., and Bryant, M. J., Involvement of endogenous opioid peptides in the neuroendocrine response of ewe lambs to the introduction of a ram. J. Endocr.115 (1987) 333–339.
Stetson, M. H., Elliott, J. A., and Goldman, B. D., Maternal transfer of photoperiodic information influences the photoperiodic response of prepubertal Djungarian hamsters. Biol. Reprod.34 (1986) 664–669.
Steiner, R. A., Metabolic cues for the onset of puberty in subhuman primates. Proc. Nutr. Soc.46 (1987) 159–175.
Tamarkin, L., Abastillas, P., Chen, H.-C., McNemar, A., and Sidbury, J. B., The daily profile of plasma melatonin in obese and Prader-Willi-syndrome children. J. clin. Endocr. Metab.55 (1982) 491–495.
Tamarkin, L., Reppert, S. M., Orloff, D. J., Klein, D. C., Yellon, S. M., and Goldman, B. D., Ontogeny of the pineal melatonin rhythm in the Syrian (Mesocricetus auratus), and Siberian (Phodopus sungoris) hamsters and in the rat. Endocrinology107 (1980) 1061–1064.
Turek, F. W., Effect of melatonin on photic-independent and photic-dependent testicular growth in juvenile and adult male golden hamsters. Biol. Reprod.20 (1979) 1119–1122.
Ueck, M., The morphogenesis of the mammalian pineal organ, in: The Pineal Gland During Development: From Fetus to Adult, p. 43–55. Eds D. Gupta and R. J. Reiter. Croom Helm, London 1986.
Vanacek, J., Pavlik, A., and Illnerova, H., Hypothalamic melatonin receptor sites revealed by autoradiography. Brain Res.435 (1987) 359–362.
Vollrath, L., The postnatal differentiation of the mammalian pineal complex, in: The Pineal Gland During Development: From Fetus to Adult, p. 56–66. Eds D. Gupta and R. J. Reiter. Croom Helm, London 1986.
Waldhauser, F., and Gisinger, B., The pineal gland and its development in human puberty, in: The Pineal Gland During Development: From Fetus to Adult, p. 134–143. Eds. D. Gupta and R. J. Reiter. Croom Helm, London 1986.
Waldhauser, F., Weizsenbacher, G., Tatzer, E., Gisinger, B., Waldhauser, M., Schemper, M., and Frisch, H., Alterations in noctural serum melatonin levels with growth and aging. J. clin. Endocr. Metab.66 (1988) 648–652.
Wallen, E. P., and Turek, F. W., Phtoperiodicity in the male albino laboratory rat. Nature289 (1981) 402–404.
Weaver, D. R., and Reppert, S. M., Maternal melatonin communicates daylength to the fetus in Djungarian hamsters. Endocrinology119 (1986) 2861–2863.
Weaver, D. R., Keohan, J. T. and Reppert, S. M., Definition of a prenatal sensitive period for maternal-fetal communication of day-length. Am. J. Physiol.253 (1987) E701-E704.
Williams, L. M., and Morgan, P. J., Demonstration of melatoninbinding sites on the pars tuberalis of the rat. J. Endocr.119 (1988) R1-R3.
Wilson, M. E., and Gordon, T. P., Season determines timing of first ovulation in outdoor-housed rhesus monkeys. J. Reprod. Fert.85 (1989) 583–591.
Wilson, M. E., and Gordon, T. P., Short-day melatonin pattern advances puberty in seasonally breeding rhesus monkeys. J. Reprod. Fert.86 (1989) 435–444.
Wilson, M. E., and Gordon, T. P., Nocturnal changes in serum melatonin during female puberty in rhesus monkeys, a longitudinal study. J. Endocr.121 (1989) 553–562.
Wilson, M. E., Gordon, T. P., Blank, M. S., and Collins, D. C., Timing of sexual maturity in female rhesus monkeys (Macaca mulatta) housed outdoors. J. Repord. Fert.70 (1984) 625–633.
Wilson, M. E., Gordon, T. P., Rudman, C. R., and Tanner, J. M., Effects of a natural verusus artificial environment on the tempo of maturation in female rhesus monkeys. Endocrinology123 (1988) 2653–2661.
Yellon, S. M., and Foster, D. L., Alternate photoperiods time puberty in the female lamb. Endocrinology116 (1985) 2090–2097.
Yellon, S. M., and Foster, D. L., Melatonin rhythms time photoperiod-induced puberty in the female lamb. Endocrinology119 (1986) 44–49.
Yellon, S. M., and Goldman, B. D., Photoperiod control of reproductive development in the male Djungarian hamster (Phodopus sungoris). Endocrinology114 (1984) 664–670.
Yellon, S. M., and Longo, L. D., Effect of maternal pinealectomy and reverse photoperiod on the circadian melatonin rhythm in the sheep and fetus during the last trimester of pregnancy. Biol. Reprod.39 (1988) 1093–1099.
Yellon, S. M., and Longo, L. D., Melatonin rhythms in fetal and maternal circulation during pregnancy in sheep. Am. J. Physiol.252 (1987) E799-E802.
Zemdegs, I. Z., McMillen, I. C., Walker, D. W., Thorburn, G. D., and Nowak, R., Diurnal rhythms in plasma melatonin concentrations in the fetal sheep and pregnant ewe during late gestation. Endocrinology123 (1988) 284–289.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ebling, F.J.P., Foster, D.L. Pineal melatonin rhythms and the timing of puberty in mammals. Experientia 45, 946–954 (1989). https://doi.org/10.1007/BF01953052
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01953052