Reprod Dom Anim 45 (Suppl. 3), 42–49 (2010); doi: 10.1111/j.1439-0531.2010.01661.
x
ISSN 0936-6768
Neuroendocrine and Genetic Control of Seasonal Reproduction in Sheep and Goats
P Chemineau1, L Bodin2, M Migaud1, JC Thiéry1 and B Malpaux1
1
INRA, UMR Physiologie de la Reproduction et des Comportements, INRA, CNRS, Haras Nationaux, Univ. F. Rabelais, Nouzilly France; 2INRA,
Station d’Ame´lioration Ge´ne´tique des Animaux Castanet Tolosan Cedex, France
Contents
Goats and sheep generally express seasonal variations in their
sexual behaviour, spermatogenic activity (from moderate
decrease to very low sperm production), gamete quality
(variations in fertilization rates and embryo survival), ovula-
tion frequency (presence or absence of ovulation), and
ovulation rate (number of eggs shed per ovulation period).
This induces seasonal availability of derived, fresh animal
products (meat, milk and cheese) because of a more or less
marked seasonal distribution of births. A complex combina-
tion of an endogenous circannual rhythm driven and synchro-
nized by light and melatonin, which controls the pulsatile
activity of GnRH neurons in the preoptic-mediobasal hypo-
thalamus, is responsible for these changes. Dramatic and
long-term neuroendocrine changes, involving different neu-
romediator systems and neuronal plasticity, have been shown
to play a role in these processes. A strong variability between
breeds exists in both species regarding the dates of onset and
end of the breeding season, with a gradient of seasonality from
southern to northern latitudes. Within a breed, seasonal traits
are heritable; thus, genetic selection could be one way to
decrease seasonality in sheep and goats in the future.
Introduction
Under temperate climates, the amount of milk in goats
and sheep and the number of kids or lambs vary greatly
throughout the year. This has dramatic consequences on
the attractiveness of these different products to the food
processing industry and ⁄ or in the price paid to produc-
ers. For example, in France, the mean monthly produc-
tion of lambs is low in October and high in April,
causing significant changes to the market price of lamb
meat. Similarly, goat milk production is highly seasonal,
ranging from over 20 million litres in November to
approximately 50 million in May, in which more than
halves the price paid to the producer in the winter
months (Chemineau et al. 2007). This pattern is because
of a more or less marked seasonal peak in births at the
most favourable period for the progeny to survive in
natural conditions, i.e. at the end of winter–early spring.
Human consumption probably adapted to the seasonal
availability of animal products for a long time before
domestication (Balasse et al. 2003, 2006). Although
seasonality is generally reduced by domestication com-
pared to wild counterparts of the domestic farm species,
sheep- and goat-derived products generally remain acces-
sible seasonally. Even after a prolonged process of
domestication, domestic stocks still show the character-
istics of the natural populations from which they origi-
nated, and cycles of reproduction and production remain
seasonal (Ortavant et al. 1985; Bronson 1989).
Because it is one of the main remaining constraints
within some domestic animal populations, we will focus
here on the neuroendocrine mechanisms involved in the
seasonal variations of reproductive activity in sheep and
goat species and on the genetic variability of this trait,
because genetic improvement for low seasonality opens
new prospects for these species.
Seasonality of Lambings and Kiddings is
Because of Changes in Gonadal Activity,
Controlled Centrally by GnRH Pulsatile
Activity
In bucks and rams, although spermatogenic activity and
sexual behaviour never stop, they vary enormously with
season. In Soay sheep, a primitive breed from North
Scotland, plasma Folliculo-stimulating hormone (FSH),
testosterone concentration, sexual ‘flush’, aggressive
behaviour and testicular size (which reflects spermato-
genic activity), reach their maximum during the ‘rut’
season, i.e. between August and November (Lincoln
1979). Sperm production per testis (directly measured at
its output) and testicular weight in Ile-de-France rams
vary from more than 5 billion per day and 300 g in
September, to <1 billion per day and 200 g in March,
respectively (Ortavant et al. 1985). Sexual behaviour
(1.5–0 mating in 10 min), individual sperm motility
(3.5–2.5 over 5) and fertilizing ability (70–20% of
kiddings after AI) also vary dramatically in Alpine
bucks between the autumn–winter and spring–summer
periods (Delgadillo et al. 1992). In this breed, seasonal
changes in ejaculate volume and sperm concentration
show a deleterious effect of seminal plasma on in vitro
sperm survival have important implications for semen
technology.
Ovulations and oestrous behaviour in Chios and
Serres ewes (Avdi et al. 1993), as well as in Ile-de-France
ewes (Thimonier and Mauléon 1969) present a period of
sexual rest during the anoestrous season even when
maintained in excellent body condition. Unmated
Alpine and Saanen dairy goats show similar variations
(Chemineau et al. 1992). In some breeds, such as Ile-
de-France and Prealpes ewes, isolated ovulations with-
out any associated behaviour are observed in some
females during the anoestrous season (Thimonier and
Mauléon 1969). In prolific breeds, ovulation rate also
varies seasonally; this is the case of Chios ewes for which
the ovulation rate is higher during the breeding season
than during the anestrus season (4.0 vs 2.0, respectively;
Fig. 1; Avdi et al. 1993).
The seasonal changes in breeding activity originate
almost exclusively from changes in luteinizing hormone
(LH) and FSH secretions from the pituitary, which is
itself controlled by GnRH pulsatility at the brain-portal
 2010 Blackwell Verlag GmbH
Seasonality of Reproduction in Small Ruminants
4 Circannual Rhythm of Reproductive
3
Ovulation rate
2 day length–specific effects are not permanent, and when
1 riod: LD are no longer inhibitory, SD are no longer
S O N D J F M A M J J A S O N D J F M A M J J
Months
Fig. 1. Seasonal variations in ovulation rate in Chios (closed circles)
and Serres (open circles) ewes from Grece (from Avdi et al. 1993)
system ⁄ pituitary level (Barrell et al. 1992). The fre-
quency of GnRH release in the portal system is the
essential message sent by the brain seasonally to control
the whole pituitary-gonadal axis.
These seasonal changes in GnRH pulsatile activity are
driven by photoperiod and melatonin, which acts to
synchronize the endogenous rhythm of reproduction.
The neuroendocrine mechanisms responsible for the
seasonal and luminous control of GnRH pulsatility
were discussed extensively by Malpaux a few years
ago (2006) and we will only give a brief overview of
the principal mechanisms involved in the present
paper.
These mechanisms can be placed into four main
groups closely interrelated with each other (Fig. 2):
1. The photoperiodic drive of reproductive activity
which has been demonstrated by numerous and
varied light-controlled experiments using inversion
of the annual cycle, long day and short day regimens,
acceleration of the annual frequency, medium-term
maintenance in constant long and short photoperiods
(which induce refractoriness) and illumination of
photosensitive phases.
2. The endogenous circannual rhythm of reproduc-
tive activity, whose existence was strongly suggested
by the results of pinealectomy, or long-term main-
tenance in constant long and ⁄ or constant short
photoperiods. This endogenous circannual rhythm
is synchronized by discrete external light signals and
could either work on a clock basis or on an
hourglass basis.
3. The neuroendocrine mechanisms of light action on
reproductive activity which have been demonstrated
to be driven via pineal melatonin secretion in the
cerebrospinal fluid (CSF), its action on the pre-
mammillary hypothalamus (PMH) probably via Mel-
atonin receptor type 1 (MT1), and the cascade of
events to GnRH control.
4. The neuroendocrine mechanisms involved in the
seasonal regulation of reproductive activity, strongly
associated with the mechanisms above, and which
were demonstrated to vary seasonally and control
GnRH pulsatile activity.
 2010 Blackwell Verlag GmbH
43
Photoperiod Synchronizes an Endogenous
Neuroendocrine Activity
It is known for a long time that long days (LD) inhibit
while short days (SD) stimulate sexual activity in short-
day breeders, such as sheep and goats. However, these
subjected to a constant photoperiod, animals become
‘refractory’, they ‘escape’ from the prevailing photope-
stimulatory. In goats and ewes, this refractoriness could
conceptually be considered as merely the first step of the
expression of the circannual endogenous rhythms. It can
be overcome (‘broken’) by transferring animals into the
opposing photoperiod: refractoriness to SD, which
occurs naturally in sheep in late winter, is broken by
2 months of exposure to LD in December–January,
allowing the efficiency of stimulatory SD to be restored
(Jackson et al. 1988).
Thus, controlling the seasonality of reproduction is
possible by subjecting animals to opposing photoperiods.
This property is now commonly used in photoperiodic
treatments applied on farms or in AI centres (Chemineau
et al. 2007). The definition of what is really LD and SD is
not straightforward: it is possible to define a threshold of
photosensitivity based on the number of light hours per
day, under which LD are stimulatory and below which
SD are inhibitory (see reviews Chemineau et al. 1996 and
Malpaux et al. 1996). It is now commonly accepted that
LD are days longer than the preceding ones, and that SD
are days shorter than the preceding ones.
As previously explained, the breeding season for a
given breed is very stable from 1 year to another, with
fixed dates of onset and offset of female ovulatory
activity and a period of maximum quantitative and
qualitative sperm production. This precise timing is
because of complex mechanisms that allow animals to
‘locate’ their breeding season over the year and express
their sexual activity at the right time, synchronously
with external environmental factors and between sexes.
In these seasonal mammals, similarly to the circadian
clock (i.e. with a free-running period close to 24 h that
generates endogenous circadian rhythms), a circannual
rhythm, endogenous to animals, is likely to generate
alternate periods of sexual rest with periods of sexual
activity throughout the year. These alternate periods can
be experimentally observed over at least two consecutive
years, when animals are kept under artificial constant
photoperiodic regimens (constant short days, for exam-
ple, Jansen and Jackson 1993; Malpaux et al. 2001;
Malpaux 2006; Gomez-Brunet et al. 2008). Sheep and
hamsters are the two experimental models that have
contributed to a better understanding of the endogenous
rhythms and refractoriness, which are essential mecha-
nisms governing seasonal reproduction (Larkin et al.
2002; Lehman et al. 2002; Paul et al. 2008) or pelage
moult (Paul et al. 2008).
In ewes, this endogenous rhythm is timed by discrete
signals given by external changes in photoperiod (Barrell
et al. 2000). However, the physiological mechanisms
underlying this circannual system remain largely
unknown.
44 P Chemineau, L Bodin, M Migaud, JC Thiéry and B Malpaux

(b)
Light
Transduction Endogenous circannual
Light --> Endocrine rhtyhm:
(a) Pineal gland Message «box» Endogenous Pinealectomy
Photoperiodic drive: Eyes circannual
Inversion of annual cycle Permanent SD
Melatonin Clock «box»
Long days-short days Permanent LD
Clock
Clockor Discrete light driving
Frequency acceleration SCN
Hourglass ? Not connected to circadian
Refractoriness to SD and to LD
Photosensitive phases CSF Thyroid gland
PMH Brain
T4
MT1 5HT2A

(c) DA
Neuroendocrine A15
NA
(d)
mechanisms of GnRH drive
«box» Neuroendocrine mechanisms of
light-action:
seasonal regulation:
Melatonin rhythm Nutritional regulation
GnRH drive
CSF route Plasticity of connexions
Changes in –ve FB of E2
Importance of PMH
KissPeptin Importance of A15 nucleus and DA
Melatonin receptors MT1
GPR54 Role of NA, DA and 5HT
GnRH control by melatonin
Brain plasticity
Permissive role of T4
Nutritional regulation
T4 window GnRH pulsatility
GnRH neurons «box» KissPeptin and GPR54
T4 acts in PMH
5HT and 5HT2A receptors
BBB and pineal gland BBB GnRH
Pituitary gland

E2 LH, FSH

Ovaries

Fig. 2. Schematic representation of the neuroendocrine control of seasonal reproductive activity in sheep and goats. The various mechanisms
were placed into four closely interacting groups (see text for more explanations). Groups (a) and (b) SD = short days, LD = long days; Group
(c) )ve FB of E2 = negative feed-back of estradiol, DA = Dopamine, NA = Noradrenalin, 5HT = Serotonin; Group (d) CSF = cerebro-
spinal fluid, PMH = Premamillary hypothalamus, MT1 = Melatonin receptor type 1, T4 = Thyroxine, 5HT = Serotonin, 5HT2A = Sero-
tonin receptor type 2A, BBB = Blood-brain-barrier, GPR54 = Kisspeptin receptor. Figure itself: SCN = Suprachiasmatic nuclei, A15 = A15
nucleus of the retrochiasmatic hypothalamus, E2 = Estradiol, LH = Luteinizing hormone, FSH = Folliculo-stimulating hormone

implants inserted within the PMH triggered GnRH-LH

Light is Transformed into a Nervous and then
Hormonal Message, Melatonin Secretion,
Which Controls the Reproductive
Neuroendocrine Activity
The photoperiodic input in mammals is perceived
exclusively through the eyes, then transmitted via a
multi-synaptic pathway to the pineal gland, which
transduces the photic signal into a chemical.
Peripheral blood melatonin concentrations are very
repeatable within ewes, but very variable between ewes;
this trait has a strong heritability, and is linked to pineal
size and weight (Chemineau et al. 2002). It is thought
that melatonin is delivered to the peripheral tissues by
the systemic circulation and to the brain via the
cerebrospinal fluid (Malpaux et al. 2001; Tricoire et al.
2002). Thiery et al. (2009) have recently shown that the
turnover rate of CSF in ewes changes according to the
light–dark cycle; it is increased during short days and
reduced in long days, thus this phenomenon could
account for differences in hormonal concentrations in
the CSF, and could to some extent affect the melaton-
ergic message to the responsive sites within the brain.
To control reproductive activity, and especially
GnRH pulsatile activity in sheep, melatonin acts on
the PMH. It was clearly demonstrated that melatonin
activity, while melatonin implants inserted within the
pars tuberalis of the pituitary (where a strong density of
melatonin receptor is expressed in ewes as in a majority
of mammals) did not (Malpaux et al. 1998). Melatonin
receptor MT1 transcripts can be detected (Migaud et al.
2005), and the membrane receptors are expressed in the
Ile-de-France sheep PMH.
Approximately 45 days after the onset of daily
melatonin impregnation (Viguié et al. 1995), these
receptors are likely to be involved in the stimulation of
the pulsatile activity of GnRH which, in turn, will drive
gonadal and behavioural sexual activities (review by
Malpaux et al. 2001; Malpaux 2006). Whereas melato-
nin acts within the PMH to control GnRH-LH pulsatile
activity, it operates within the pars tuberalis to control
seasonal prolactin secretion. In the pars tuberalis,
melatonin stimulates a complex signalling pathway
which involves different ‘clock’ genes (Lincoln 2002;
Hazlerigg et al. 2004; Hanon et al. 2008).
The neural network connecting hypothalamic mela-
tonin receptor bearing cells of the PMH and GnRH
neurons is probably very complex and could also be
responsible for the long delay in the action of melatonin
on GnRH pulsatility (Viguié et al. 1995). In sheep,
dopaminergic activity inhibits the GnRH pulsatility

 2010 Blackwell Verlag GmbH

Seasonality of Reproduction in Small Ruminants
probably at the end of the network, in the median
eminence (Thiery et al. 1989; Viguie et al. 1997),
through D2 receptors (Bertrand et al. 1999). Interest-
ingly, in hamsters, dopamine from the median eminence
is also correlated with the inhibition of gonadotropin
release (Steger et al. 1985; Glass et al. 1988).
Pelletier and Ortavant (1975) identified a spontaneous
seasonal change in the negative feedback (FB) potency
of gonadal steroids (strong FB in anoestrus season) as
one of the key elements of the system. Changes in
plasma LH pulsatility and mean concentration, which
are parallel to the expression of ovulations in ovary-
intact ewes, are observed in ovariectomized, estradiol
implanted ewes (low LH pulsatility and low LH medium
concentration during the anoestrus season vs high LH
pulsatility and high LH medium concentration during
the ovulatory season; Legan and Karsch 1980; Karsch
et al. 1984). Seasonal changes in the steroid transport
from the periphery to the brain via changes in the
blood–brain barrier permeability could be responsible
for a part of the mechanism (Thiery and Malpaux 2003;
Thiery et al. 2006), but the main part of the phenom-
enon probably takes place in various specific hypotha-
lamic areas bearing identified or putative estradiol
receptors. The dopaminergic (DA) A15 nucleus of the
retrochiasmatic hypothalamus is probably a key-nucleus
in the network between estradiol binding cells and
GnRH neurons of the preoptic area (Thiery et al. 1989,
1995). Interestingly, these estradiol binding cells are
100
E#4098
Plasma LH (ng/ml)
10
1 (p < 0.01)
100
E#4111
Plasma LH (ng/ml)
10
Jul Sep Dec Mar Jun
1996 1997
Fig. 3. 5HT2A receptor gene expression (mRNA) and 5HT2A protein binding (Ket binding) in two phases of the endogenous circannual rhythm
(top: high LH pulsatility and high mean LH plasma concentrations vs low LH pulsatility and low mean LH plasma concentrations) in ovx + E2
pinealectomized Suffolk ewes (from Chemineau et al. 2003)
 2010 Blackwell Verlag GmbH
45
located in dual sites, the retrochiasmatic hypothalamus
itself (Gallegos-Sánchez et al. 1997) and the ventral
preoptic area (Anderson et al. 2001). Within the A15
nucleus, DA neurons are contacted by glutamatergic
terminals, and the number of close contacts is signif-
icantly higher in anoestrus than during the breeding
season (Singh et al. 2009).
In ewes, seasonal plasticity, identified by changes in
Poly-Sialated Neural Cell Adhesion Molecule (PSA-
NCAM), has been demonstrated. The expression of
PSA-NCAM immunoreactivity associated with GnRH
neurons was significantly greater during the breeding
season than that during the anestrus season, in the
preoptic area, around the periphery of GnRH cell
bodies (Viguié et al. 2001; Lehman et al. 2002). Con-
current seasonal changes identified by synapsin expres-
sion have been shown in the A15 nucleus, this latter
plasticity depending upon thyroid hormone (Adams
et al. 2006). Similarly, increases in the expression and
binding capacity of serotoninergic receptor 5HT2A in
the PMH were observed in association with high
pulsatile LH activity during active phases of refractory
states compared to inactive phases (Le Corre et al. 1994;
Chemineau et al. 2003; Fig. 3).
Thyroxine or T4 plays a permissive role and needs to
be present at a constantly low plasma level during
seasonal transitions (Dahl et al. 1995; Billings et al.
2002); it acts centrally in the ewe brain (Viguié et al.
1999).
40
3H-Ketanserin binding (fmol/mg of protein)
5HT2A receptor mRNA (grains/neuron)
20 30
(p < 0.05)
0
1 2 3 4
20
40
20
10
0
1 2 3 4
Hours
0
mRNA Ket binding
Sep Dec Mar June
1998
46
More recently, the stimulatory role of kisspeptin and
its receptor GPR54 was shown in the seasonal (Clarke
et al. 2009; Smith et al. 2009) and photoperiodic (Chali-
voix et al. 2010) control of GnRH ⁄ LH pulsatility,
suggesting that this couple plays a key role for the
stimulation of pulsatility and that kisspeptin neurons
themselves are subjected to seasonal and photoperiodic
control.
Inter- and Intra-breed Variability Indicates the
Existence of a Genetic Control of Reproductive
Seasonality
Among sheep and goat species, variable degrees of
seasonality are expressed by the various breeds. For
example, Merino and Manchega ewes (Santiago-
Moreno et al. 2000) as well as Chios ewes (Avdi et al.
1993), present moderate expression of seasonality, while
Soay and Texel ewes are highly seasonal (Hafez 1952).
In the tropics, local breeds generally present a very low
seasonality, or cycle all the year round with no anovu-
latory period (Gonzalez-Stagnaro 1983; Khaldi 1984;
Yenikoye 1984; Chemineau 1986; Mahieu et al. 1989;
Arroyo et al. 2007). Farmers in the tropics are interested
by this low seasonality as they can then organize the
breeding season of their flock all the year round, without
expensive hormonal treatments. Unfortunately, when
subjected to the large photoperiodic variations and
temperate climates of northern countries, a marked
seasonality is expressed in these breeds (Chemineau
et al. 2004; Fig. 4). This prevents their possible practical
use in flocks under temperate latitude and also impairs
their experimental use to explore the mechanisms
involved in the genetic control of seasonality of breeding
activity under temperate latitudes.
Intra-breed variability also exists in temperate breeds
maintained under environmental conditions similar
from which they originate. Some reproductive traits
including the onset, offset and duration of the breeding
Tropical
photoperiod
100
80
% of goats showing at least
one ovulation per month
60
40
20
Temperate
photoperiod
0
O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J
Year 1
Fig. 4. Ovulatory activity of tropical Creole meat goats submitted to a tropical (closed circles) or to a temperate (open circles) photoperiodic
regimen (from Chemineau et al. 2004)
P Chemineau, L Bodin, M Migaud, JC Thiéry and B Malpaux
season were found repeatable and heritable, and are
therefore candidate traits for genetic selection (Ricordeau
1982; Quirke et al. 1986; Hanrahan 1987; Smith et al.
1992). Out-of-season fertility was also shown to be a trait
which can be used for successful divergent selection (Al-
Shorepy and Notter 1997; Notter 2008). To avoid the
deleterious effects of selecting experimentally against
fertility (which is difficult for flock renewal), indirect traits
such as the presence of spontaneous ovulatory activity in
early spring, which probably indicates a longer breeding
season and is linked to potential fertility, was found to be
heritable in Merino ewes (Hanocq et al. 1999) and could
be used in selection. In this breed, divergent selection on
this trait is feasible (Teyssier et al. 2002). Such lines could
be used in the future to explore in more detail the intimate
mechanisms by which seasonal breeds control their
annual reproductive ability and the genes involved in this
control.
Unfortunately, the results for the neuroendocrine
mechanisms which were investigated to explain this
genetic variability in the characteristics of the breeding
season were relatively disappointing. As stated earlier,
plasma melatonin concentration has a strong heritability
and is linked to pineal size and weight (Chemineau et al.
2002). Selection for out-of-season fertility was demon-
strated to be associated with a decrease in nocturnal
melatonin plasma concentration, which may suggest a
link between nocturnal melatonin amplitude and sea-
sonality (Notter and Chemineau 2001). However, prob-
ably because the melatonin signal from the pineal gland
to the PMH is transduced via direct liberation into the
CSF and not via the general circulation (Tricoire et al.
2002), this genetic variability in melatonin secretion is
not linked to the variability in either the onset or the
offset of the breeding season (Zarazaga et al. 2003). The
demonstration of a significant relationship between
intensity of anovulation (presence ⁄ absence of spontane-
ous out-of-season ovulations) and the relative frequency
of precise alleles of the melatonin receptor MT1 in
Year 2 Year 3
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Seasonality of Reproduction in Small Ruminants
Merino sheep was shown and suggests that using this
polymorphism could be used for selecting animals on
the presence of favourable alleles (Pelletier et al. 2000;
Notter et al. 2003; Notter and Cockett 2005). However,
the association between the frequency of MT1 alleles
and the characteristics of the ovulatory season (onset,
offset and duration) was not found subsequently when
two groups of homozygous Ile-de-France ewes born
from the same heterozygous sires were compared
(Hernandez et al. 2005).
To our knowledge, there has not been any other
attempt to explore the neuroendocrine mechanisms
which may explain the genetic variability of seasonality
of breeding activity in sheep.
Thus, this genetic variability, as it occurs for many
other traits, is probably not dependent on the polymor-
phism of a single gene but rather on a variety of genes
most of which still remain to be identified and assessed
prior to any possible direct application in selection.
Conclusion
The seasonality of small ruminant product availability is
not a deliberate choice of the farmer to produce at a
definite season, but rather the consequence of interac-
tions between the natural endogenous rhythmicity of
animals and environmental constraints. Even though
various and numerous neuroendocrine mechanisms
were elucidated in the last decades and have deepened
understanding of the ways by which ewes and goats
initiate then stop their seasonal breeding activity, the
whole chain of events is not known. To propose
selection criteria and ⁄ or gene markers accessible to
primary breeder and producer organizations willing to
reduce seasonality in their flocks will only be possible
after an elucidation of the biological bases underlying
the strong genetic variability of seasonal reproductive
activity in the main farm animal species.
Acknowledgement
The authors thank Dr John Williams for his corrections of the
manuscript.
Conflicts of interest
Authors declare the absence of any financial and personal relationships
with other people or organisations (employment, consultancies, stock
ownership, honoraria, paid expert testimony, or direct or indirect
funding) that could inappropriately bias or influence their work.
Author contributions
PC wrote the first version of this manuscript which was corrected and
amended later on by LB, MM, JCT and BM.
References
Adams VL, Goodman RL, Salm AK, Coolen LM, Karsch FJ,
Lehman MN, 2006: Morphological plasticity in the neural
circuitry responsible for seasonal breeding in the ewe.
Endocrinology 147, 4843–4851.
 2010 Blackwell Verlag GmbH
47
Al-Shorepy SR, Notter DR, 1997: Response to selection for
fertility in a fall-lambing sheep flock. J Anim Sci 75, 2033–2040.
Anderson GM, Connors JM, Hardy SL, Valent M, Goodman
RL, 2001: Oestradiol microimplants in the ventromedial
preoptic area inhibit secretion of luteinizing hormone via
dopamine neurones in anoestrous ewes. J Neuroendocrinol
13, 1051–1058.
Arroyo LJ, Gallegos-Sanchez J, Villa-Godoy A, Berruecos
JM, Perera G, Valencia J, 2007: Reproductive activity of
Pelibuey and Suffolk ewes at 19 north latitude. Anim
Reprod Sci 102, 24–30.
Avdi M, Driancourt MA, Chemineau P, 1993: Variations
saisonnières du comportement d’oestrus et de l’activité
ovulatoire chez les brebis Chios et Serres en Grèce. Reprod
Nutr Dev 33, 15–24.
Balasse M, Smith AB, Ambrose SH, Leigh SR, 2003:
Determining sheep birth seasonality by analysis of tooth
enamel oxygen isotope ratios: the Late Stone Age site of
Kasteelberg (South Africa). J Archaeol Sci 30, 205–215.
Balasse M, Tresset A, Ambrose SH, 2006: Stable isotope
evidence (¶13C, ¶18O) for winter feeding on seaweed by
Neolithic sheep of Scotland. J Zool 270, 170–176.
Barrell GK, Moenter SM, Caraty A, Karsch FJ, 1992:
Seasonal changes of gonadotropin-releasing hormone
secretion in the ewe. Biol Reprod 46, 1130–1135.
Barrell GK, Thrun LA, Brown ME, Viguie C, Karsch FJ,
2000: Importance of photoperiodic signal quality to entrain-
ment of the circannual reproductive rhythm of the ewe. Biol
Reprod 63, 769–774.
Bertrand F, Thiery JC, Picard S, Malpaux B, 1999: Implica-
tion of D2-like dopaminergic receptors in the median
eminence during the establishment of long-day inhibition
of LH secretion in the ewe. J Endocrinol 163, 243–254.
Billings HJ, Viguie C, Karsch FJ, Goodman RL, Connors JM,
Anderson GM, 2002: Temporal requirements of thyroid
hormones for seasonal changes in LH secretion. Endocri-
nology 143, 2618–2625.
Bronson FH, 1989: Mammalian reproductive biology. The
University of Chicago press Ltd., Chicago and London 325 p.
Chalivoix S, Bagnolini A, Caraty A, Cognie J, Malpaux B,
Dufourny L, 2010: Effects of photoperiod on Kisspeptin
neuronal populations of the ewe diencephalon in connection
with reproductive function. J Neuroendocrinol 22, 110–118.
Chemineau P, 1986: Sexual behaviour and gonadal activity
during the year in the tropical Creole meat goat. I. Female
oestrous behaviour and ovarian activity. Reprod Nutr Dev
26, 441–452.
Chemineau P, Daveau A, Maurice F, Delgadillo JA, 1992:
Seasonality of oestrus and ovulation is not deeply modified
by submitting Alpine goats to a tropical photoperiod. Small
Ruminant Res 8, 299–312.
Chemineau P, Malpaux B, Pelletier J, Leboeuf B, Delgadillo
JA, Deletang F, Pobel T, Brice G, 1996: Emploi des
implants de mélatonine et des traitements photopériodiques
pour maı̂triser la reproduction saisonnière chez les ovins et
les caprins. Prod Anim 9, 45–60.
Chemineau P, Daveau A, Bodin L, Zarazaga L, Gomez-
Brunet A, Malpaux B, 2002: The sheep as a mammalian
model of plasma melatonin variability. Reproduction Suppl
59 (Large Mammals as Neuroendocrine Models), 181–190.
Chemineau P, Daveau A, Pelletier J, Malpaux B, Karsch FJ,
Viguie C, 2003: Changes in the 5-HT2A receptor system in the
pre-mammillary hypothalamus of the ewe are related to
regulation of LH pulsatile secretion by an endogenous
circannual rhythm. BMC Neurosci 4, 1 (http://www.biomed
central.com/1471-2202/4/1).
Chemineau P, Daveau A, Cognie Y, Aumont G, Chesneau D,
2004: Seasonal ovulatory activity exists in tropical Creole
48
female goats and Black Belly ewes subjected to a temperate
photoperiod. BMC Neurosci 4, 12 (http://www.biomed
central.com/1472-6793/4/12).
Chemineau P, Malpaux B, Brillard JP, Fostier A, 2007:
Seasonality of reproduction and production in farm fishes,
birds and mammals. Animal 1, 419–423.
Clarke IJ, Smith JT, Caraty A, Goodman RL, Lehman MN,
2009: Kisspeptin and seasonality in sheep. Peptides 30, 154–
163.
Dahl GE, Evans NP, Thrun LA, Karsch FJ, 1995: Thyrox-
ine is permissive to seasonal transitions in reproductive
neuroendocrine activity in the ewe. Biol Reprod 52, 690–
696.
Delgadillo JA, Leboeuf B, Chemineau P, 1992: Abolition of
seasonal variations in semen quality and maintenance of
sperm fertilizing ability by short photoperiodic cycles in he-
goats. Small Ruminant Res 9, 47–59.
Gallegos-Sánchez J, Delaleu B, Caraty A, Malpaux B,
Thiéry JC, 1997: Estradiol acts locally within the retro-
chiasmatic area to inhibit pulsatile luteinizing-hormone
release in the female sheep during anestrus. Biol Reprod
56, 1544–1549.
Glass JD, Ferrera S, Deaver DR, 1988: Photoperiodic adjust-
ment in hypothalamic amines gonadotrophin-releasing
hormone and b-endorphin in white -footed mouse. Endo-
crinology 123, 1119–1127.
Gomez-Brunet A, Santiago-Moreno J, del Campo A, Malpaux
B, Chemineau P, Tortonese DJ, Gonzalez-Bulnes A, Lopez-
Sebastian A, 2008: Endogenous circannual cycles of ovarian
activity and changes in Prolactin and Melatonin secretion in
wild and domestic female sheep maintained under a Long-
Day photoperiod. Biol Reprod 78, 552–562.
Gonzalez-Stagnaro C, 1983: Comportamiento reproductivo de
las razas locales de rumiantes en el tropico americano. In:
Reproduction des ruminants en zone tropicale. Chemineau
P, Gauthier D, Thimonier J, Versailles Fr (Eds). Inra
Publications 20, 1–84.
Hafez ESE, 1952: Studies on the breeding season and
reproduction of the ewe. J Agric Sci 42, 189–265.
Hanocq E, Bodin L, Thimonier J, Teyssier J, Malpaux B,
Chemineau P, 1999: Genetic parameters of spontaneous
spring ovulatory activity in Merinos d’Arles sheep. Genet
Sel Evol 31, 77–90.
Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-
Pevet M, Morgan PJ, Hazlerigg DG, 2008: Ancestral TSH
mechanism signals summer in a photoperiodic mammal.
Curr Biol 18, 1147–1152.
Hanrahan JP, 1987: Genetic variation in seasonal reproduc-
tion in sheep. Proceedings 38th Annual Meeting of the
European Association for Animal Production, Lisbon,
Portugal, September 28 – October 1, 14P.
Hazlerigg DG, Andersson H, Johnston JD, Lincoln G, 2004:
Molecular characterization of the long-day response in the
Soay sheep, a seasonal mammal. Curr Biol 14, 334–339.
Hernandez X, Bodin L, Chesneau D, Guillaume D, Chemi-
neau P, Malpaux B, Migaud M, 2005: Relationship between
MT1 melatonin receptor gene polymorphism and seasonal
physiological responses in Ile-de-France ewes. Reprod Nutr
Dev 45, 151–162.
Jackson GL, Gibson M, Kuehl D, 1988: Photoperiodic
disruption of photorefractoriness in the ewe. Biol Reprod
38, 127–134.
Jansen HT, Jackson GL, 1993: Circannual rhythms in the
ewe: patterns of ovarian cycles and prolactin secretion
under two different constant photoperiods. Biol Reprod 49,
627–634.
Karsch FJ, Bittman EL, Foster DL, Goodman RL, Legan SJ,
Robinson JE, 1984: Neuroendocrine basis of seasonal
reproduction. Recent Prog Horm Res 40, 185–232.
P Chemineau, L Bodin, M Migaud, JC Thiéry and B Malpaux
Khaldi G, 1984: Variations saisonnières de l’activité ovarienne,
du comportement d’oestrus et de la durée de l’anoestrus
post-partum des femelles ovines de race Barbarine : influ-
ence du niveau alimentaire et de la présence du mâle. PhD
Thesis, University of Montpellier, France, 168 p.
Larkin JE, Jones J, Zucker I, 2002: Temperature dependence
of gonadal regression in Syrian hamsters exposed to short
day lengths. Am J Physiol Regul Integr Comp Physiol 282,
R744–R752.
Le Corre S, Segu L, Caldani M, Chemineau P, 1994:
Differences in Ketanserin binding in the ventromedial
hypothalamus of ewes responsive or refractory to short
days. Neuroendocrinology 60, 589–600.
Legan SJ, Karsch FJ, 1980: Photoperiodic control of seasonal
breeding in ewes: modulation of the negative feedback
action of estradiol. Biol Reprod 23, 1061–1068.
Lehman MN, Coolen LM, Goodman RL, Viguie C, Billings
HJ, Karsch FJ, 2002: Seasonal plasticity in the brain: the use
of large animal models for neuroanatomical research.
Reprod Suppl 59 (Large Mammals as Neuroendocrine
Models), 149–165.
Lincoln G, 1979: Photoperiodic control of seasonal breeding in
the ram: participation of the cranial sympathetic nervous
system. J Endocrinol 82, 135–147.
Lincoln GA, 2002: Neuroendocrine regulation of seasonal
gonadotrophin and prolactin rhythms: lessons from the
Soay ram model. Reprod Suppl 59, (Large Mammals as
Neuroendocrine Models) 131–147.
Mahieu M, Jego Y, Driancourt MA, Chemineau P, 1989:
Reproductive performances of Creole and Black-Belly ewes
in the West Indies. A new major gene controlling ovulation
rate? Anim Reprod Sci 19, 235–243.
Malpaux B, 2006: Seasonal regulation of reproduction in
mammals. in: Neill JD(Ed), Knobil and Neill’s Physiology
of Reproduction, 3rd edition, Elsevier, Amsterdam, pp.
2231–2281.
Malpaux B, Viguie C, Thiery JC, Chemineau P, 1996:
Contrôle photopériodique de la reproduction. Prod Anim
9, 9–23.
Malpaux B, Daveau A, Maurice-Mandon F, Duarte G,
Chemineau P, 1998: Evidence that melatonin acts in the
pre-mammillary hypothalamic area to control reproduction
in the ewe: presence of binding sites and stimulation of LH
secretion by in situ microimplant delivery. Endocrinology
139, 1508–1516.
Malpaux B, Migaud M, Tricoire H, Chemineau P, 2001:
Biology of mammalian photoperiodism and the critical role
of the pineal gland and melatonin. J Biol Rhythms 16, 336–
347.
Migaud M, Daveau A, Malpaux B, 2005: MTNR1A melato-
nin receptors in the ovine premammillary hypothalamus:
day-night variation in the expression of the transcripts. Biol
Reprod 72, 393–398.
Notter DR, 2008: Genetic aspects of reproduction in sheep.
Reprod Dom Anim 43(Supp 2), 122–128.
Notter DR, Chemineau P, 2001: Nocturnal melatonin and
prolactin plasma concentrations in sheep selected for fertil-
ity in autumn lambing. J Anim Sci 79, 2895–2901.
Notter DR, Cockett NE, 2005: Opportunities for detection
and use of QTL influencing seasonal reproduction in sheep:
a review. Genet Sel Evol 37(Suppl 1), S39–S53.
Notter DR, Cockett NE, Hadfield TS, 2003: Evaluation of
melatonin receptor 1a as a candidate gene influencing
reproduction in an autumn-lambing sheep flock. J Anim
Sci 81, 912–917.
Ortavant R, Pelletier J, Ravault JP, Thimonier J, Volland P,
1985: Photoperiod: main proximal and distal factor of the
circannual cycle of reproduction in farm mammals. Oxf Rev
Reprod Biol 7, 305–345.
 2010 Blackwell Verlag GmbH
Seasonality of Reproduction in Small Ruminants
Paul MJ, Zucker I, Schwartz WJ, 2008: Tracking the seasons:
the internal calendars of vertebrates. Philos Trans R Soc
Lond B Biol Sci. 2008 Jan 27 363(1490): 341–361. Review.
Pelletier J, Ortavant R, 1975: Photoperiodic control of LH
release in the ram. II. Light-androgens interaction. Acta
Endocrinol (Copenh) 78, 442–450.
Pelletier J, Bodin L, Hanocq E, Malpaux B, Teyssier J,
Thimonier J, Chemineau P, 2000: Association between
expression of reproductive seasonality and alleles of the gene
for mei1a receptor in the ewe. Biol Reprod 62, 1096–1101.
Quirke JF, Hanrahan JP, Loughnane W, Triggs R, 1986:
Components of the breeding and non-breeding seasons in
sheep: breed effects and repeatability. Irish J Agr Food Res
25, 167–172.
Ricordeau G, 1982: Selection for reduced seasonality and post-
partum anoestrus. In 2nd World Congress of Genetics
Applied to Livestock Production, Madrid, Spain, 5, 338–
347.
Santiago-Moreno J, Lopez-Sebastian A, Gonzalez-Bulnes A,
Gomez-Brunet A, Chemineau P, 2000: Seasonal changes in
ovulatory activity, plasma prolactin, and melatonin concen-
trations, in Mouflon (Ovis gmelini musimon) and Manchega
(Ovis aries) ewes. Reprod Nutr Dev 40, 421–430.
Singh SR, Hileman SH, Connors JM, McManus CJ, Coolen
LM, Lehman MN, Goodman RL, 2009: Estradiol negative
feedback regulation by Glutamatergic afferents to A15
dopaminergic neurons: variation with season. Endocrinol-
ogy 150, 4663–4671.
Smith JF, Johnson DL, Reid TC, 1992: Genetic parameters
and performance of flocks selected for advanced lambing
date. Proceedings of the New Zealand Society of Animal
Production 52 50 (Abstr).
Smith JT, Saleh SN, Clarke IJ, 2009: Seasonal and cyclical
change in the luteinizing hormone response to kisspeptin in
the ewe. Neuroendocrinology 90, 283–291.
Steger RW, Matt KS, Klemke HG, Bartke A, 1985: Interac-
tions of photoperiod and ectopic graphs on hypothalamic
and pituitary function in male hamsters. Neuroendocrinol-
ogy 41, 89–96.
Teyssier J, Canepa S, Chemineau P, Malpaux B, Migaud M,
Bodin L, 2002: Preliminary results on selection lines for
spontaneous spring ovulatory activity in merinos d’arles
sheep. 7th World Congress on Genetics Applied to
Livestock Production Montpellier 19–23 August, p. 685–
688.
Thiery JC, Malpaux B, 2003: Seasonal regulation of repro-
ductive activity in sheep: modulation of access of sex
steroids to the brain. Ann N Y Acad Sci 1007, 169–175.
Thiery JC, Martin GB, Tillet Y, Caldani M, Quentin M,
Jamain C, Ravault JP, 1989: Role of hypothalamic cate-
cholamines in the regulation of luteinizing hormone and
prolactin secretion in the ewe during seasonal anestrus.
Neuroendocrinology 49, 80–87.
 2010 Blackwell Verlag GmbH
49
Thiery JC, Gayrard V, Le Corre S, Viguie C, Martin GB,
Chemineau P, Malpaux B, 1995: Dopaminergic control of
LH secretion by the A15 nucleus in anoestrous ewes. J
Reprod Fertil Suppl 49, 285–296.
Thiery JC, Lomet D, Schumacher M, Liere P, Tricoire H,
Locatelli A, Delagrange P, Malpaux B, 2006: Concentra-
tions of estradiol in ewe cerebrospinal fluid are modulated
by photoperiod through pineal-dependent mechanisms. J
Pineal Res 41, 306–312.
Thiery JC, Lomet D, Bougoin S, Malpaux B, 2009: Turnover
rate of cerebrospinal fluid in female sheep: changes related
to different light-dark cycles. Cerebrospinal Fluid Res 6, 6–
9.
Thimonier J, Mauléon P, 1969: Variations saisonnières du
comportement d’oestrus et des activités ovariennes et
hypophysaires chez les ovins. Ann Biol Anim Bioch Biophys
9, 233–250.
Tricoire H, Locatelli A, Chemineau P, Malpaux B, 2002:
Melatonin enters the cerebrospinal fluid through the pineal
recess. Endocrinology 143, 84–90.
Viguie C, Thibault J, Thiery JC, Tillet Y, Malpaux B, 1997:
Characterization of the short day-induced decrease in
median eminence tyrosine hydroxylase activity in the ewe:
temporal relationship to the changes in luteinizing hormone
and prolactin secretion and short day-like effect of melato-
nin. Endocrinology 138, 499–506.
Viguié C, Caraty A, Locatelli A, Malpaux B, 1995: Regulation
of luteinizing hormone-releasing hormone (GnRH) secre-
tion by melatonin in the ewe. I. Simultaneous delayed
increase in GnRH and luteinizing hormone pulsatile secre-
tion. Biol Reprod 52, 1114–1120.
Viguié C, Battaglia DF, Krasa HB, Thrun LA, Karsch FJ,
1999: Thyroid hormones act primarily within the brain to
promote the seasonal inhibition of luteinizing hormone
secretion in the ewe. Endocrinology 140, 1111–1117.
Viguié C, Jansen HT, Glass JD, Watanabe M, Billings HJ,
Coolen L, Lehman MN, Karsch FJ, 2001: Potential for
polysialylated form of neural cell adhesion molecule-medi-
ated neuroplasticity within the gonadotropin-releasing hor-
mone neurosecretory system of the ewe. Endocrinology 142,
1317–1324.
Yenikoye A, 1984: Annual variations in estrual behavior, rate
and possibilities for ovulation in Peulh ewes from Niger.
Reprod Nutr Dev 24, 11–19.
Zarazaga LA, Malpaux B, Chemineau P, 2003: Amplitude of
the plasma melatonin rhythm is not associated with the
dates of onset and offset of the seasonal ovulatory activity in
the Ile-de-France ewe. Reprod Nutr Dev 43, 167–177.
Author’s address (for correspondence): Philippe Chemineau, INRA
Physiologie de la Reproduction et des Comportements, INRA, CNRS,
Haras Nationaux, Univ. F. Rabelais, 37380 Nouzilly, France. E-mail:
philippe.chemineau@tours.inra.fr