Is a Critical Interval of the Circadian Pacemaker at Dusk Responsive to Light and Melatonin Responsible for the Timing of Estrus in the Romney Marsh Ewe?

Abstract

Two experiments, using Romney Marsh ewes, tested for the existence and role of a critical interval of the circadian pacemaker located near dusk that may be integrally involved in the precise timing of the breeding season. Groups of Romney Marsh ewes (n = 6) were provided with exogenous melatonin by injection at dusk (Experiment 1) or by infusion at dawn or subjected to extended darkness at dawn (Experiment 2) from the winter to the summer solstice before being exposed to natural photoperiod at latitude 35 degrees S. Other than the experimental protocols, all animals were held in natural photoperiod. The onset of the breeding season (defined as cyclic ovarian activity as indicated by plasma progesterone monitoring) was normal in those animals treated with morning melatonin but was delayed in those animals treated with melatonin at dusk or extended darkness at dawn compared to controls in natural photoperiod (p < .01). Exogenous melatonin at dusk was associated with a phase advance of the onset of the circadian pacemaker (as measured by endogenous melatonin in acutely extended darkness); additional darkness at dawn was associated with a phase delay of both the onset and the offset of the circadian pacemaker. Exogenous morning melatonin did not change the phase of the circadian pacemaker relative to the controls. The results are consistent with an external coincidence model of seasonal breeding in which a critical interval of the circadian pacemaker requires exposure to light during spring/summer to time estrus correctly. The proposed critical interval appears to be located near dusk in this model and is phase locked to the circadian pacemaker. The effect of the exogenous melatonin on the timing of the breeding season is similar to darkness when administered at dusk but is not equivalent to darkness at dawn. The timing of anestrus was not affected by any of the experimental treatments and may reflect a common response to an environmental influence.

Alterations of Estrous Activity in the Ewe by Circadian-Based Manipulation of the Endogenous Pacemaker

“…All results for the control group (Group A) are comparable to those reported previously for control groups in similar studies (Guerin et al, 1994;Matthews et al, 1995). The onset and offset times for each group of elevated endogenous melatonin measured under the different treatment photoperiods reflected closely the dark period on all occasions.…”

“…The onset of anestrous was taken as the date of the last progesterone value above baseline at the completion of the cycling progesterone pattern, also determined as the number of days from the 1991 summer solstice for statistical comparisons. In practice, the rise was readily identified and definable as elevated values typically were 10 to 20 times higher than the minimum detectable level (Matthews et al, 1995).…”

“…The onset (and offset) of the melatonin rise was defined as the initial sample obtaining a meaningful detectable (undetectable) melatonin level above (below) the assay sensitivity provided that subsequent samples sustained the rise (or absence of rise). In practice, the elevated melatonin level typically was three to four times the assay sensitivity; hence, the rise and fall were readily determined (Matthews et al, 1995).…”

“…Such a hypothesis largely conforms to the "external coincidence" model of Pittendrigh and Minis (1964) with light as the zeitgeber and the photosensitive phase located about the time of natural dusk. When the exposure of dusk light to the photosensitive phase is blocked (by either additional darkness or the administration of exogenous melatonin) before the summer solstice, the onset of the subsequent breeding season is delayed (Guerin et al, 1994;Matthews et al, 1995). Thus, any failure of the normal reception of the dusk light signal during the natural long photoperiod can alter the timing of the subsequent breeding season.…”

“…Melatonin secretion has been investigated extensively to understand its role in the precise timing of seasonal estrous, and most studies have supported the nightly duration of melatonin secretion, which varies throughout the year, as the crucial mechanism (for a review, see Karsch et al, 1991), the so-called duration model. Alternative explanations have invoked a phase coincidence mechanism postulating either a melatoninsensitive phase (Rollag et al, 1978) or a photoreceptive phase sensitive to both natural light and melatonin (Matthews et al, 1995). The precise interplay between melatonin and the photoperiod that controls the annual timing mechanism remains unclear.…”