Reproduction in Domestic Animals

Seasonality of Reproduction in Mammals 43reproduction (Larkin et al. 2002; Lehman et al. 2002;Paul et al. 2008) or pelage moult (Paul et al. 2008). Thisendogenous rhythm is timed, in ewes, by discrete signalsgiven by external changes in photoperiod (Barrell et al.2000). However, the specific physiological mechanismsunderlying this circannual system remain largely unknown.The specific role of short days (SD) and long days(LD) days in timing reproductive activity varies amongspecies. In long-day breeders (i.e. animals which arefully sexually active during LD) like horses, LD arestimulatory and SD inhibitory of sexual activity. Incontrast, LD inhibit while SD stimulate sexual activityin short-day breeders such as sheep and goats. Howeverin mammals subjected to a constant photoperiod, thedaylength-specific effect is not permanent. Animals‘escape’ and become ’refractory’ to the prevailing photoperiod:LD are no longer stimulatory in mares orinhibitory in sheep and goats, SD are no longerinhibitory in mares or stimulatory in sheep and goats.This refractoriness could conceptually be considered asmerely the first step of the expression of the circannualendogenous rhythm. It can be ‘broken’ by transferringanimals into the opposite photoperiod: refractoriness toSD, which occurs naturally in sheep in late winter, isbroken by 2 months of exposure to LD in December–January, allowing the efficiency of stimulatory SD to berestored. Thus, by subjecting animals to oppositephotoperiods, it is possible to control seasonality ofreproduction. This property is now commonly used inphotoperiodic treatments applied on farms and ⁄ or inAI centres (see below). The definition of what is reallyLD and SD is not straightforward: it is possible todefine a threshold of photosensitivity based on thenumber of light hours per day, under which LD arestimulatory and below which SD are inhibitory (seereviews Chemineau et al. 1996 and Malpaux et al.1996). The ‘photoperiodic history’ of each individualshould also be taken into account. Thus, it is nowcommonly accepted that LD are days longer than thepreceding ones, and that SD are days shorter than thepreceding ones. This property is interesting under fieldconditions: following a period of artificial long days,animals perceive SD even though natural daylength islonger than 12 h of light per day. Another interestingproperty can be used under farm conditions to applylong days: the illumination of a specific phase of thenight, the so-called ‘photosensitive phase’, generallysituated 14–16 h after dawn in sheep and 9.5 h afterdusk in mares, allows animals to perceive LD eventhough real LD are not applied (see reviews of Malpauxet al. 1996; Chemineau et al. 1996 in sheep and goats,and Guillaume 1996 in mares).More generally, photoperiod, which entrains theendogenous circannual rhythms of reproduction, exertsits action through two different but complementary anddependent pathways by (1) adjusting the phases ofgonadal development with external natural conditionsand (2) by synchronizing the reproductive periodbetween individuals of the same species. In mammals,all the photoperiodic input is perceived exclusivelythrough the eyes then transmitted via a multi-synapticpathway to the pineal gland, which transduces thephotic signal into a chemical one by synthesizing andsecreting melatonin. Synthesized during the night by thepineal gland, it is thought that melatonin is delivered tothe brain via the cerebrospinal fluid, and to peripheraltissues by general circulation. To control reproductiveactivity in sheep, melatonin acts on the pre-mammillaryhypothalamus where specific receptors transcripts areexpressed (Migaud et al. 2005) and the membranereceptor is present, which stimulates, approximately45 days after the onset of daily impregnation (Viguie´et al. 1995), the pulsatile activity of LHRH-LH which inturn will drive gonadal and behavioural sexual activities(review by Malpaux 2006; Malpaux et al. 2001). Externalmelatonin can be given to ‘mimic’ short days and hasbeen of practical use in sheep and goats to stimulatereproduction in spring. Details of the neuroendocrinemechanisms responsible for the seasonal and lightcontrol of LHRH pulsatility could not be discussedextensively here (see Malpaux 2006 for an extensivereview), especially what differs between short-day breeders(sheep and goats) and long-day breeders (horses andhamsters) to explain their opposite change in LHRHneuron pulsatility to the same melatonin signal. However,it is likely that the difference lies in the neuralnetwork connecting hypothalamic melatonin receptorbearing cells and LHRH neurones, a network that isalso responsible for the long delay of action of melatoninon LHRH pulsatility (Viguié et al. 1995). Forexample, dopaminergic activity inhibits the LHRHpulsatility at the end of the neural network during longdays in sheep (Thiery et al. 1989). Interestingly, dopaminefrom the median eminence is also correlated withthe inhibition of gonadotropin release, which takes placeunder short days in these species (Steger et al. 1985;Glass et al. 1988).Although molecular mechanisms underlying the centralcontrol of gonadotrope system by melatonin stillconstitute a ‘black box’, numerous experiments usingonly photoperiodic variations have lead to proposals tofarmers and artificial insemination centres of specificlight devices, which may be able to control seasonalityof reproduction of their animals.Using Artificial Photoperiodic Treatments toControl Seasonality of Reproduction in FarmAnimalsPhotoperiodic treatments have been of practical interestfor controlling seasonal reproduction essentially insheep, goats and horses. Sheep and goat AI centres,equipped with dark housing, use alternate light regimeswith 1 month LD and 1 month SD which allowpermanent high semen production in rams and bucks,with no seasonal variations in sperm quality. Currently,in the French national genetic improvement scheme, allbucks (approximately 70 per year) are permanentlytreated with rapid alternation LD–SD, which increasesthe AI dose production (+40%) per buck and per year(Delgadillo et al. 1993) and reduces duration of thebreeding period of males (slaughtered after 18 monthsof production, or approximately 18 months earlier thatthose maintained under natural photoperiod). In otherAI centers which do not require all the year-roundÓ 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag