The Coincidence of Light and Melatonin with a Specific Phase of the Circadian Pacemaker Is Important for the Timing of Seasonal Breeding in the Ewe

Abstract

The timing of reproductive activity in seasonal breeding sheep relies on daily photoperiodic signals being relayed to provide information on the time of year. Although light and melatonin are involved, the exact mechanism is not understood. In this experiment, three groups of 6 Romney Marsh ewes, a highly seasonal breed, were provided with 8 weeks of short nights (9.6-9.8 h, by artificially advancing dawn) around the winter solstice, near the end of their natural breeding season. One group of animals was infused to a physiological level with melatonin for 5 h during the afternoon prior to the onset of dark, while a second group was identically infused but for 5 h from the time of lights on. A third group received the short-night treatment only. Following the short-night treatment, all groups were exposed to long nights (> 14 h, by delaying dawn) until the summer solstice. Ovarian activity, assessed by progesterone monitoring twice weekly, showed that the noninfused and the morning-infused groups displayed renewed reproductive activity in response to the short-night/long-night treatment. There was no renewed ovarian activity in the afternoon-infused group, indicating that the time of day that melatonin is present, rather than the duration of melatonin exposure, is an important signal in the control of reproductive timing. Measurements of a marker of the endogenous circadian pacemaker, by melatonin measurements under acutely extended darkness, revealed that the short-night treatments phase advanced the onset of the pacemaker in all groups such that the afternoon phase of the pacemaker was coincident with light. The results provide strong support for the model that proposes that an afternoon-located sensitive phase of the pacemaker is responsible for the relay of photoperiodic signals in the timing control of seasonal breeding. The model proposes that the reproductive axis be primed during short nights when the sensitive phase is coincident with light in the afternoon so ovarian activity can be induced when the sensitive phase is located within the longer nights of autumn and coincident with endogenous melatonin.

Annual pattern of plasma melatonin and progesterone concentrations in hair and wool ewe lambs kept under natural photoperiod at lower latitudes in the southern hemisphere

“…No seasonal differences were observed in blood samples collected before (17:00 hr) or after (8:00 hr) the annual dusk and dawn times respectively (Table 3). These results are in agreement with those existing in the literature, which have demonstrated that all seasonal changes, which characterize the classic annual pattern of plasma melatonin concentration, occur during the nocturnal times [26,27,29,30].…”

“…In our study, it was not possible to determine exactly the rise times of elevated melatonin, but it could be inferred that the rise times of elevated melatonin were at or after dusk when seasonal differences were evidenced. In fact, the onset of melatonin is clearly delayed relative to dusk at all times of year as ewes were kept under natural or artificial photoperiod at 35°S in Australia and this delay was significantly greater in winter [26,30,31]. Although the difference in winter night (13.3 hr) and summer night (10.7 hr) at the latitude of the present study is only 2.6 hr, the model of annual melatonin secretion of wool and hair sheep seems to be the same of those raised under natural or artificial conditions in intermediate or high latitudes in southern or northern hemispheres.…”

“…The plasma progesterone concentrations were lower in RM females. Peripheral progesterone concentrations have been used to monitor the cyclic reproductive activity in sheep [17, 28–30, 32, 33]. Ewes were judged to be in anovulation if plasma progesterone concentration never exceeded 1 ng/mL for more than two consecutive samples or during a 10‐day period [17, 33].…”

Melatonin concentrations in the two jugular veins, and relationship with the seasonal reproductive activity in goats

“…Two main alternative hypotheses have been proposed to explain how nycthemeral melatonin secretion controls reproductive activity: the duration of the melatonin secretion, and the temporal phase of this rise relative to the light-dark cycle have both been considered [7][8][9][10]. For each hypothesis, the amplitude of melatonin secretion may play a specific role to modulate the response; it has been suggested that the ratio nocturnal/diurnal melatonin after implant insertion [11] or under natural conditions [12] could be related to the speed of resumption of ovulatory activity.…”

The antidepressant‐like effect of the melatonin receptor ligand luzindole in mice during forced swimming requires expression of MT2 but not MT1 melatonin receptors

“…The hormone melatonin is synthesized and secreted foremost by the mammalian pineal gland following a distinct circadian rhythm with the acrophase during the dark phase, and the nadir during the light phase in both diurnal and nocturnal species [1]. Melatonin modulates a number of physiological, behavioral and neuroendocrine functions in mammals including sleep promotion [2], phase shift and entrainment of circadian rhythms [3–5], and reproduction in seasonal breeders [6, 7]. There is growing evidence suggesting a role for melatonin in the pathophysiology of affective disorders, namely, depression.…”