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• W2034646859 abstract "For many animals, knowing the time of year and predicting the forthcoming season is crucial for their survival and that of their offspring. Recent research sheds light on hormonal mechanisms that perform this calendar function in birds and mammals. For many animals, knowing the time of year and predicting the forthcoming season is crucial for their survival and that of their offspring. Recent research sheds light on hormonal mechanisms that perform this calendar function in birds and mammals. How does our brain know when to wake up in the morning? Dr. Seuss' Chippendale Mupp has an amusing method of timing such daily activities. It has an extraordinarily long (and, presumably, non-myelinated) tail, which it bites just prior to going to sleep. According to Dr. Seuss, its tail is so long that it doesn't feel any pain until the “nip makes the trip” to its brain exactly 8 hours later and causes it to wake up with a yell. This simple, yet effective, biological circuit might allow the Chippendale Mupp to know when it is morning, but how could it tell which season it was in? What are the local environmental conditions going to be like in three months? Should it try and hoard food? Breed? Migrate? Get fat? These are real, life-or-death challenges that wild animals face on an annual basis. Daily, or circadian, activity in vertebrates is timed by the suprachiasmatic nucleus (SCN) in the brain [1Stephan F.K. Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions.Proc. Nat. Acad. Sci. USA. 1972; 69: 1583-1586Crossref PubMed Scopus (1483) Google Scholar, 2Moore R.Y. Eichler V.B. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat.Brain Res. 1972; 42: 201-206Crossref PubMed Scopus (1538) Google Scholar] and we now know a great deal about SCN biology. In contrast, timing of seasonal processes is less well understood. In all vertebrates, the hormone melatonin is secreted from the pineal gland at night, so the duration of the night (or day) dictates the duration of melatonin secretion. Thus, the melatonin signal provides organisms with a very accurate measurement of both the length of the day and whether the day lengths are increasing (spring) or decreasing (fall). Knowing this, one can rightly expect that many seasonally breeding animals use the nightly melatonin signal to time seasonally appropriate changes in their reproductive physiology and behavior. Melatonin is important for timing seasonal processes such as gonadal growth and regression, but not all animals respond to it in the same way. Some mammals (e.g., sheep and deer) mate during short days and their young are born during the lengthening days the following spring. Other mammals with shorter gestation periods (e.g., hamsters and voles) mate and give birth solely during the long days of spring and summer. Melatonin administration to these animals (as an endocrine mimic of short days) has rapid and profound effects on their reproductive status. Short-day breeders, such as sheep, undergo gonadal activation and long-day breeders, such as hamsters, exhibit gonadal inactivation, but they all have one thing in common: melatonin duration provides time of year information to coordinate reproduction. Unlike in mammals, there is little evidence of a direct role for melatonin in the regulation of gonadal function in birds. Removal of the pineal gland and the eyes (the retina is also a significant source of melatonin in birds) does not alter the gonadal response to changing day length in American tree sparrows [3Wilson F.E. Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea).J. Exp. Zool. 1991; 259: 117-127Crossref Scopus (93) Google Scholar]. In some experiments, melatonin stimulates gonadal growth in birds [4Juss T.S. Meddle S.L. Servant R.S. King V.M. Melatonin and photoperiodic time measurement in Japanese quail (Coturnix coturnix japonica).Proc. Biol. Sci. 1993; 254: 21-28Crossref PubMed Google Scholar] and, in others, it inhibits gonadal growth [5Balasubramanian K.S. Saxena R.N. Effect of pinealectomy and photoperiodism in the reproduction of Indian weaver birds, Ploceus phillipinus.J. Exp. Zool. 1973; 185: 333-340Crossref PubMed Scopus (35) Google Scholar]. As such, there has been no unifying ‘melatonin theme’ in terms of a timing mechanism for seasonal breeding in birds and mammals. Thyroid hormones have also been implicated in seasonal breeding. Removal of the thyroid gland in sheep, deer and several bird species completely disrupts seasonal changes in activity of the reproductive system, often prematurely inducing gonadal growth in birds [6Wieselthier A.S. van Tienhoven A. The effect of thyroidectomy on testicular size and on the photorefractory period in the starling (Sturnus vulgaris L.).J. Exp. Zool. 1972; 179: 331-338Crossref PubMed Scopus (97) Google Scholar, 7Dawson A. Williams T.D. Nicholls T.J. Thyroidectomy of nestling starlings appears to cause neotenous sexual maturation.J. Endocrinol. 1987; 112: R5-R6Crossref PubMed Google Scholar], sheep [8Moenter S.M. Woodfill C.J.I. Karsch F.J. Role of the thyroid gland in seasonal reproduction: Thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes.Endocrinology. 1991; 128: 1337-1344Crossref PubMed Scopus (123) Google Scholar, 9Parkinson T.J. Douthwaite J.A. Follett B.K. Responses of prepubertal and mature rams to thyroidectomy.J. Reprod. Fert. 1995; 104: 51-56Crossref PubMed Scopus (24) Google Scholar] and red deer [10Shi Z.D. Barrell G.K. Requirement of thyroid function for the expression of seasonal reproductive and related changes in red deer (Cervus elaphus) stags.J. Reprod. Fert. 1992; 94: 251-259Crossref PubMed Scopus (67) Google Scholar]. So, if melatonin and thyroid hormones are important for timing of seasonal breeding, how do they interact? The pars tuberalis (PT) of the pituitary might be a key component of the interaction between melatonin and thyroid hormones. The first of several recent findings that pointed to such a role for the PT was that, in quail mediobasal hypothalamus, long day lengths induce the gene encoding type 2 iodothyronine deiodinase (Dio2), an enzyme which activates thyroid hormone [11Yoshimura 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: 178-181Crossref PubMed Scopus (358) Google Scholar] (Figure 1A). Thus, long days increase conversion of thyroxine (T4) into its bioactive form, tri-iodothyronine (T3), to about 10-fold higher than under short-day conditions. In addition, infusion of T3 into the brain induced testicular growth in quail held under non-stimulatory short days. Activation of Dio2 is one of the earliest events detected in the photoperiodic cascade. These effects on gene activation are thought to amplify the localized action of thyroid hormones and lead to neuroendocrine changes that cause secretion of gonadotropin-releasing hormone (GnRH) a few hours later. GnRH then causes release of gonadotropins, luteinizing hormone (LH) and follicle-stimulating hormone (FSH) from the anterior pituitary gland, activating the gonads. The mechanism by which thyroid hormones are processed and transferred to the GnRH system is not yet known. Very recently, a wave of thyrotropin (TSH) β-subunit gene expression in the PT was identified even earlier than activation of Dio2 at hour 14 of a single long day [12Nakao N. Ono H. Yamamura T. Anraku T. Takagi T. Higashi K. Yasuo S. Katou Y. Kageyama S. Uno Y. et al.Thyrotrophin in the pars tuberalis triggers photoperiodic response.Nature. 2008; 452: 317-322Crossref PubMed Scopus (344) Google Scholar]. Central administration of TSH to short-day quail stimulated gonadal growth and expression of Dio2. Thus, there appears to be a role for the PT and TSH in the regulation of T3 and the avian photoperiodic response. How melatonin might fit into this scenario is not yet known, but a study on Soay sheep by Hanon et al. [13Hanon E.A. Lincoln G. Fustin J.-M. Dardente H. Masson-PévetMorgan P.J. Hazelrigg D.G. Ancestral TSH mechanism signals summer in a photoperiodic mammal.Curr. Biol. 2008; 18: 1147-1152Abstract Full Text Full Text PDF PubMed Scopus (265) Google Scholar], in a recent issue of Current Biology, might provide us with a new perspective. In that study, a similar effect on Dio2 and TSH by long days was identified in the PT of Soay sheep [13Hanon E.A. Lincoln G. Fustin J.-M. Dardente H. Masson-PévetMorgan P.J. Hazelrigg D.G. Ancestral TSH mechanism signals summer in a photoperiodic mammal.Curr. Biol. 2008; 18: 1147-1152Abstract Full Text Full Text PDF PubMed Scopus (265) Google Scholar], but the effect was much slower than in quail (10 days after the onset of long days, versus hours in quail) (Figure 1B). Collectively, these recent findings have the potential to revolutionize our understanding of vertebrate seasonal breeding. It is not yet known how the photoperiod signal is relayed to the pituitary and the hypothalamus to regulate TSH and Dio2, but the ovine PT expresses melatonin receptors. Thus, the daily melatonin rhythm could provide day-length information to the hypothalamus via effects on TSH release from the PT. As Hanon et al. [13Hanon E.A. Lincoln G. Fustin J.-M. Dardente H. Masson-PévetMorgan P.J. Hazelrigg D.G. Ancestral TSH mechanism signals summer in a photoperiodic mammal.Curr. Biol. 2008; 18: 1147-1152Abstract Full Text Full Text PDF PubMed Scopus (265) Google Scholar] point out, the TSH-expressing cells of the PT might be part of an ancestral mechanism by which photoperiodic information is conveyed to the reproductive axis, although a mechanism for transmission of the day-length signal to the PT in quail still remains unclear and melatonin microimplants around the PT in some sheep have little effect on LH release [14Malpaux B. Daveau A. Maurice F. Locatelli A. Thiéry J.C. Evidence that melatonin binding sites in the pars tuberalis do not mediate the photoperiodic actions of melatonin on LH and prolactin secretion in ewes.J. Reprod. Fertil. 1994; 101: 625-632Crossref PubMed Scopus (43) Google Scholar]. However exciting and potentially important these recent findings might be from the perspectives of ecology, physiology and evolution, it's obvious that they do not provide us with the full picture. For example, how is this common mechanism tweaked so as to cause short-day breeding in some species and long-day breeding in others? Also, we again have the avian/mammalian dichotomy in terms of the nature of their respective reproductive responses to melatonin. Furthermore, many mammals and birds, unlike Soay sheep, have hypothalamic melatonin receptors. Quail express melatonin receptors on a set of hypothalamic neurons that directly inhibits reproductive activity [15Ubuka T. Bentley G.E. Ukena K. Wingfield J.C. Tsutsui K. Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain.Proc. Natl. Acad. Sci. USA. 2005; 102: 3052-3057Crossref PubMed Scopus (246) Google Scholar]. Hypothalamic melatonin implants in several mammals, including Soay sheep, are sufficient to elicit reproductive responses, and ablating hypothalamic areas abolishes melatonin's effects upon reproduction [16Lincoln G.A. Administration of melatonin into the mediobasal hypothalamus as a continuous or intermittent signal affects the secretion of follicle stimulating hormone and prolactin in the ram.J. Pineal Res. 1992; 12: 135-144Crossref PubMed Scopus (28) Google Scholar, 17Freeman D.A. Zucker I. Refractoriness to melatonin occurs independently at multiple brain sites in Siberian hamsters.Proc. Natl. Acad. Sci. USA. 2001; 98: 6447-6452Crossref PubMed Scopus (56) Google Scholar, 18Maywood E.S. Hastings M.H. Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotropic, but block the gonadotropic response of male Syrian hamsters to short photoperiod and to melatonin.Endocrinology. 1995; 136: 144-153PubMed Google Scholar, 19Hileman S.M. Kuehl D.E. Jackson G.L. Effect of anterior hypothalamic area lesions on photoperiod-induced shifts in reproductive activity of the ewe.Endocrinology. 1994; 135: 1816-1823PubMed Google Scholar]. Thus, many vertebrates have a functional hypothalamic system with which they can potentially interpret day-length changes and regulate seasonal endocrinology and behavior via a more ‘classic’ pathway than the newly identified Dio2 pathway. Perhaps in vivo manipulations of Dio2 expression will help to clarify its role in seasonal timing. Despite these caveats, it seems that these recent studies on Dio2 regulation via the PT bring us closer to understanding mechanisms of seasonal timing in birds and mammals. Because of the varied nature of the vertebrate photoperiodic response, it will be hard to identify a truly unifying mechanism. Thus, I'll reverse one of Dr. Seuss' sayings and end with: “Sometimes the questions are simple and the answers are complicated.”" @default.
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• W2034646859 date "2008-09-01" @default.
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• W2034646859 title "Biological Timing: Sheep, Dr. Seuss, and Mechanistic Ancestry" @default.
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