Small Ruminant Research 48

Small Ruminant Research 48 (2003) 155–171
Review
Seasonality of reproduction in sheep
H.J.D. Rosa a,∗, M.J. Bryant b
a Departamento de Ciˆencias Agrárias, Universidade dos Açores, Angra do Heroismo, 9701-851 Portugal
b Department of Agriculture, University of Reading, Whiteknights, P.O. Box 236, Reading RG6 6AT, UK
Received 28 January 2002; received in revised form 1 November 2002; accepted 24 December 2002
Abstract
Unlike most domestic livestock species, sheep are widely known as an animal with marked
seasonality of breeding activity.
The annual cycle of daily photoperiod has been identified as the determinant factor of this
phenomenon, while environmental
temperature, nutritional status, social interactions, lambing date and lactation period are
considered to modulate it. The aim of
this paper is to reviewthe current state of knowledge of the reproductive seasonality in sheep.
Following general considerations
concerning the importance of seasonal breeding as a reproductive strategy for the survival of
species, the paper describes the
manifestations of seasonality in both the ram and the ewe. Both determinant and modulating
factors are developed and special
emphasis is given to the neuroendocrine base of photoperiodic regulation of seasonal
breeding. Other aspects such as the role
of melatonin, the involvement of thyroid hormones and the concept of photorefractoriness are
also reviewed.
© 2003 Elsevier Science B.V. All rights reserved.
Keywords: Sheep; Reproduction; Seasonality; Photoperiod; Melatonin; Anoestrus
1. Introduction
Animals live under the influence of seasonal fluctuations of environmental conditions,
with variable amplitudes frequently more marked in the higher latitudes and altitudes. The
daily photoperiod and theannual cycles in environmental temperature are the most striking
examples in temperate regions while the annual cycle in rainfall, with the consequent cycles
in food availability, are important variables in tropical regions (Vivien-Roels and Pévet,
1983). As these changes reach acute levels, the animal species may respond by developing a
series of different strategies (e.g. changing feeding habits, laying down energy reserves in the
form of fat tissue, lowering the basal metabolism, moulting skin, fur and plumage,
hibernating and migrating). Another mechanism is a reproductive strategy involving a
‘natural contraceptive method’ (Lincoln and Short, 1980) which restricts the reproductive
activity to the best time of the year for assuring that births occur at a time that promotes
maximal growth and development of the offspring and supports lactation in the mother
(Wayne et al., 1989). In cold and temperate regions, this period corresponds to spring or early
summer while in hot arid climates it coincides with the rainy season. In order to synchronise
their fertile period, seasonal breeders rely on environmental cues. Of the many environmental
variables available, photoperiod is the most commonly used synchronising agent (Karsch et
al., 1984) because unlike other climatic variables such as temperature and rainfall, the
seasonal cycle of day length is constant between years. Species that use photoperiod to
synchronise breeding activity are commonly classified in two different categories; long-day
breeders or short-day breeders. Species in the first group, which include the ferret, the
hedgehog and the horse, enter their breeding season after the winter solstice when the day
length increases. Species in the second group, such as deer, goats and sheep, become sexually
active in response to decreasing day length in the late summer to early autumn.
It is important to stress that seasonal reproduction occurs mainly in wild species as a
result of natural selection while animal domestication and artificial selection has contributed
to minimise the effects of season on reproductive activity. This idea is supported by the study
of Lincoln et al. (1990) who compared the reproductive seasonality of wild, feral and
domesticated breeds of sheep kept under similar conditions at the same latitude and
concluded that wild-type rams reached the peak of testicular activity later in the year than
domesticated rams while the feral type followed an intermediate pattern. On the other hand,
domestic species that breed throughout the year such as cattle and pigs, if left in the feral state
for an extended period, gain a strong tendency for parturition to be seasonal (Ortavant et al.,
1985).
It is clear from the literature that sheep breeds originating from temperate climates in
mid or high latitudes are seasonal breeders and use the annual variation in daily photoperiod
in timing the annual reproductive cycle. On the other hand, in tropical and sub-tropical
environments ewes are either completely aseasonal or intermittently polyoestrus with the
quality and availability of food dictating breeding activity. Supported by the works of Hafez
(1952), Goot (1969) and Dyrmundsson (1978), Robinson (1981) argues that breeds whose
origins are located between 35◦N and 35◦S have the tendency to breed at all times of the year
while at latitudes greater than 35 ◦ it is normal to find ewes that are seasonally polyoestrus
and whose breeding seasons are initiated by declining day length. In general, the higher the
latitude the greater the photodependence and the more restricted the peri od of breeding
activity (Poulton, 1987).
In this view, while tropical breeds are sexually active throughout the year, British
breeds demonstrate a distinct seasonality with a long anoestrous period during which no ewes
ovulate spontaneously. Breeds from intermediate latitudes, such as the Australian Merino and
Mediterranean breeds, have a short anoestrus during which a proportion of ewes ovulate
spontaneously (5% in Australian Merino; Martin et al., 1986).Within breeds there is also a
large variation. As an example, some ewes of the breed Préalpes-du-Sud have a very short
breeding season while others are almost aseasonal (Thimonier et al., 1986). The breeding
season starts in most ovine breeds during summer or early autumn (Chemineau et al., 1992)
and its length varies largely among breeds but in general it ends during the winter (Hafez,
1952).
2. Manifestation of seasonality in the ewe
Reproductive seasonality in the ewe is characterised by changes at behavioural,
endocrine and ovulatory levels, in an absolute fashion, giving rise to an annual alternation
between two distinct periods; a breeding season, characterised by the succession at regular
intervals (mean of 17 days) of oestrous behaviour
and ovulation, if a pregnancy does not develop, and
an anoestrous season characterised by the cessation
of sexual activity. The transition from anoestrous to
breeding season is gradual, with the occurrence of
short cycles, because the first corpus luteum (CL) often
regresses prematurely 5–6 days after its formation.
Both ovulatory activity and oestrous behaviour show
parallel seasonal variation but there are some discrepancies
at the beginning and at the end of the sexual
season when some ovulations are not accompanied
by oestrus. It is only after the end of the first ovarian
cycle that the behavioural oestrus is exhibited. Silent
ovulations, not related either to the onset or the end
of the sexual season, may also occur in some breeds
during mid-anoestrus (Land et al., 1973; Ortavant
et al., 1988). At the endocrine level, it is known that
during the anoestrous season, follicle growth and regression
occur and follicles as large as those found
during the luteal phase of the oestrous cycle may be
present (Hutchinson and Robertson, 1966; Matton
et al., 1977; Webb and Gauld, 1985). Throughout
seasonal anoestrus, the follicles produce steroids, and
many of the positive and negative feedback effects of
the steroids on secretion of luteinizing hormone (LH)
continue as in the breeding season (Gordon, 1997).
LH continues to be released, episodically, but with
lower frequency than during the reproductive season
(one pulse every 8–12 h against one pulse per 3–4 h
H.J.D. Rosa, M.J. Bryant / Small Ruminant Research 48 (2003) 155–171 157
in the mid-luteal phase, one pulse per 1–2 h immediately
prior to the preovulatory LH surge and one
pulse every 20 min during the preovulatory LH surge
(Yuthasastrakosol et al., 1977; Karsch, 1984; Martin,
1984; I’Anson and Legan, 1988; Thiéry and Martin,
1991). A major difference occurs also in plasma progesterone
concentration which remains virtually at
undetectable levels during anoestrus (Roche et al.,
1970; Karsch, 1984; I’Anson and Legan, 1988).
Follicle-stimulating hormone (FSH) levels seems not
to be significantly different from those found during
the reproductive season (Goding et al., 1969; Roche
et al., 1970; Walton et al., 1977).
3. Manifestation of seasonality in the ram
Rams exhibit seasonal fluctuations in sexual behaviour,
hormonal activity, gametogenesis and also
in testicular weight and volume (Schanbacher and
Lunstra, 1976; Lincoln and Davidson, 1977; Ortavant
et al., 1985). However, behavioural and physiological
variations are less pronounced than in the ewe.
In fact, while ovulation and oestrus in the ewe is arrested,
spermatogenesis and sexual activity in the ram
never stop. Generally, all these parameters are high
at the end of the summer and in autumn and low at
the end of winter and in spring (Lincoln and Short,
1980; Haynes and Schanbacher, 1983; Pelletier and
Almeida, 1987). Taking the Ile-de-France ram as an
example and considering that similar tendencies have
been observed in many other breeds, Ortavant et al.
(1988) report that the testis weight can vary from
180–190 to 300–320 g and spermatozoa production
per gram of testicular parenchyma can increase from
8.5 × 106 to 12.2 × 106, resulting in a daily sperm
production variation per testis of 1×109 to 4.8×109.
In Soay rams, LH and FSH levels begin to increase
2–4 weeks after the decrease in photoperiod, followed
almost immediately by a rise in plasma testosterone
levels accompanied by growth of the testis (Lincoln
and Davidson, 1977). Rams’ sensitivity to photoperiod
is different from ewes. Sexual activity is usually
stimulated 1–1.5 months earlier in rams, allowing that
when the cyclic period of the ewes starts, the rams
have already achieved a high level of sexual activity
(this advancement is important because while anoestrous
ewes can ovulate within a few days after hormonal
stimulation due to the ever present large-sized
follicles, the rams need approximately 45 days to
complete spermatogenesis).
4. Modulating factors of seasonal breeding
It is well established that seasonal reproduction in
sheep is mainly regulated by photoperiod. However,
other cues from the environment (temperature, nutrition
and social relationships) are believed to modulate
its effect. While in temperate regions the photoperiod
is the decisive factor and other environmental factors
can only influence the onset and the duration of the
anoestrous period, in tropical areas nutritional level is
probably responsible for some seasonal acyclicity.
Environmental temperature cannot impose seasonality
on reproductive activity of the ewe as was
clearly demonstrated by Wodzicka-Tomaszewska
et al. (1967). These authors found that in spite of dramatic
changes in temperature, the annual rhythm of
reproduction persisted in ewes kept under a constant
photoperiodic schedule of 12 h of light–12 h of dark
per day. However, temperature may modify the onset
of sexual season. It has been shown that ewes maintained
under low temperatures during the summer
period began their reproductive season earlier than
those kept under temperatures typical of that season
(Dutt and Bush, 1955; Godley et al., 1966). Also,
Lees (1966) found a positive correlation between
mean temperature in July and the date of the onset of
the breeding season in Clun ewes.
It is well known that nutrition affects many aspects
of reproductive performance in sheep, e.g. age
at puberty in both sexes, fertility, ovulation rate,
embryo survival, parturition to re-breeding interval,
testis growth and spermatozoa production (for details
see Smith, 1991; Clarke and Tilbrook, 1992; Rhind,
1992; Robinson, 1996). Nutritional inadequacies can
show their effects as short, middle and long-term.
Thus, while some studies indicated that ewes can
lose body weight without any immediate detrimental
effect on reproductive performance, the accumulated
losses over several reproductive cycles increase the
incidence of barrenness (Robinson, 1981). The nutritional
level received by ewes during the winter and
spring can influence the percentage of ewes showing
oestrus the following autumn (Smith, 1966) but a
158 H.J.D. Rosa, M.J. Bryant / Small Ruminant Research 48 (2003) 155–171
sub-maintenance diet introduced before the onset did
not delay the breeding season except in very young
and very old ewes (Hafez, 1952). Forcada et al. (1992)
found that the length of seasonal anoestrus was clearly
reduced when Rasa Aragonesa ewes were maintained
with low body condition score (2.5 as compared
to 2.7) for two consecutive years. Thimonier et al.
(1986) reported that the variations in the occurrence
of births in regions where the rainfall is very variable
can be explained by variations in food availability.
In contrast, Gordon (1997) concluded that both in
temperate and tropical breeds, the nutritional level
appears to have little effect on the onset and duration
of the breeding season. Robinson (1981) suggested
that some conflicting reports in this matter can be resolved
on the basis that reductions in body weight at
mating of up to 15% have little detrimental effects in
the short-term but reduce long-term production. In the
ram, changes in nutrition lead to profound responses
in testicular size and spermatogenic function (Martin
and Walkden-Brown, 1995).
The mechanisms by which dietary nutrients regulate
reproductive parameters are complex, not yet well
understood and are the subject of speculation (Parr,
1987; Smith, 1991; Robinson, 1996). However, there
are sound arguments to favour the hypotheses that
feeding regimen affects the secretion or clearance of
gonadotropins (effect on ovulation rate; Adams et al.,
1997), the clearance of progesterone (effect on pregnancy
rate; Parr, 1987) or the balance between FSH
secretion and gonadal feedback by changing the responsiveness
to the inhibitory effects of oestradiol
and inhibin (effect on seasonality of reproduction;
Boukhliq et al., 1996).
The reproductive season can also be influenced by
lambing date. The onset and duration of the natural
breeding season is affected by previous lambing date.
An early lambing date is associated with an early
onset of the subsequent breeding season (Haresign,
1992; Mitchell et al., 1997), but not with its cessation
(Mitchell et al., 1997).
Lactation period is another factor that can affect
the breeding season. Under normal conditions, in
highly seasonal breeds, births occur during seasonal
anoestrus and therefore in this situation lactational
anoestrus cannot be identified. But when the ewes are
induced to breed during seasonal anoestrus they lamb
in the breeding season and in lactating animals the
resumption of ovarian activity is known to be delayed
(Mallampati et al., 1971). Suckling has also a pronounced
effect on the length of postpartum anoestrus
in less seasonal breeds lambing naturally during the
breeding season (Shevah et al., 1974; Pope et al.,
1989). Denervation of the mammary gland has been
proved to shorten the length of postpartum anoestrus
(Kann and Martinet, 1975).
Social interactions can strongly affect the reproductive
state of sheep. Relationships between and within
sexes have been identified as influencing various parameters
of reproduction in both the ewe and the ram.
For details see the reviews of Thimonier et al. (2000)
and Rosa and Bryant (2002).
5. The photoperiod as the determinant factor
of seasonal reproduction in sheep
5.1. Experimental evidence
The role of day length as the deterministic factor in
inducing and suppressing sexual activity in both the
female and the male sheep has been clearly demonstrated
in a variety of experiments. Artificial reversal
of the annual rhythm of photoperiodic variations induces
reversal of the period of ovulatory and oestrous
activity in the ewe (Yates, 1949; Thwaites, 1965;
Wodzicka-Tomaszewska et al., 1967) and of the periods
of recrudescence and regression of testicular size
(Alberio and Colas, 1976, reported by Ortavant et al.,
1988) and sperm production in rams (Colas et al.,
1985). The treatment of animals with a light regimen
which mimics in 6 months the normal annual day
length pattern, generate in the ewe two reproductive
seasons (Ortavant and Thibault, 1956, reported by
Pelletier and Almeida, 1987) and in the rams two
cycles of testicular growth (Lindsay et al., 1984) and
sperm production (Jackson and Williams, 1973) in 1
year. Finally, the alternation of 3- or 4-month periods
of constant long (16 h of light–8 h of dark) and constant
short (8 h of light–16 h of dark) days induces the
alternation of periods of sexual activity and inactivity
in the ewe (Legan and Karsch, 1980) and testicular
growth in the ram (Lincoln and Davidson, 1977). If
the periods of day length are alternated every month,
rams show a progressive increase in testicular weight
which finally remains steady close to the maximum
level (Pelletier and Almeida, 1987). Different light
protocol treatments which produced changes in reproductive
activity in both sexes can also be seen in
the review of Chemineau et al. (1992).
5.2. Neuroendocrine mechanisms involved in the
photoperiodic control of reproduction
The answer to the intriguing question of what causes
ovulation to cease during seasonal anoestrus requires a
full understanding of the hormonal patterns and mechanisms
involved in the governing of ovarian activity
during not only the period of anoestrus but also the
periods of transition to anoestrus and return to oestrus.
The present section will focus on these points and conclude
with the presentation of the current model of the
neuroendocrine regulation of seasonal anoestrus.
5.2.1. Hormonal pattern during the transition to
seasonal anoestrus
One of the first attempts to characterise the hormonal
changes during the period of transition from
cyclicity to seasonal anoestrus in ewes was made by
Rawlings et al. (1977). These authors did not detect
any gradual changes in the concentrations of LH,
oestradiol and progesterone, but noted that at the end
of the last cycle some ewes experienced a subnormal
rise in LH concentration after which both LH
and oestradiol levels remained basal. In more elaborate
studies Karsch et al. (1980) and Legan et al.
(1981) found that the pattern of LH secretion following
the regression of the last CL of the reproductive
season is different from those of previous luteolyses.
While during the breeding season the basal LH level
increases in a sustained way for 48 h, during transition
to anoestrus it starts to increase for the first 24 h but
falls progressively in the next 24 h. In addition, there
is no occurrence of oestradiol rise and LH surge.
5.2.2. Hormonal pattern during seasonal
anoestrus
A brief description of the hormonal relationships
during the non-breeding season and some bibliographic
support has already been presented in
Section 2. Throughout this period the levels of progesterone
remain low and no gonadotrophins surges
are observed. However, neither the ovary nor the
LH pulse generating system are inactive. Follicular
development does not stop, periods of early follicle
growth and regression are taking place and mature
follicles are present. The study of follicular dynamics
by ultrasonography has shown the existence of
waves of follicular development (Souza et al., 1997).
The follicles produce steroids, and are capable of
ovulating. Gonadotrophin hormones are secreted and
both positive and negative feedback effects of ovarian
steroids on gonadotrophin secretion are readily
demonstrable (Legan and Karsch, 1979). Oestradiol
secretion is similar to the breeding season, that is an
oestradiol rise follows each LH pulse (Scaramuzzi
and Baird, 1977). In fact, the follicles are responsive
to gonadotrophin stimulation and ovulation can
occur if anoestrous ewes are treated with exogenous
gonadotrophin-releasing hormone (GnRH) (Haresign
et al., 1975; Southee et al., 1988) or multiple injections
of LH (McNeilly et al., 1982). However, the
LH pulse generating system, although active, is compromised
because both frequencies of GnRH (Barrell
et al., 1992) and LH (Karsch, 1984) are extremely
low, tending to be even less than during the luteal
phase of the cycle and sustained increases in tonic LH
secretion are not normally observed (Scaramuzzi and
Baird, 1977). Barrell et al. (1992) found that in marked
contrast with observations made during the breeding
season, an increased pulse frequency of both GnRH
and LH hormones is not observed in anoestrus, which
leads to the conclusion that the switch from breeding
to anoestrous season in the ewe is associated with a
marked change in the GnRH neurosecretory system.
5.2.3. Hormonal pattern during the transition
from anoestrous to the breeding season
Yuthasastrakosol et al. (1973) first reported data
suggesting the occurrence of minor LH surges during
late anoestrus and the existence of a rise in progesterone
levels commencing 11–15 days before the
first behavioural oestrus. In a more elaborate work,
Yuthasastrakosol et al. (1975) determined the levels of
oestrogen, progesterone and LH throughout anoestrus
and the first oestrous cycle of the breeding season.
Once again, exceptionally high levels of LH were observed
in late anoestrus, more precisely on day 24
before oestrus and minor rises of progesterone also occurred
around this period. I’Anson and Legan (1988),
using a more frequent blood sampling regime, also
confirmed the occurrence of these brief increments in
LH and progesterone levels before the first full-length
luteal phase of the breeding season. In this study, 75%
of the observed increases in LH pulse frequency occurred
within 1 week after a low frequency pattern of
secretion (full anoestrus) and within 1 week before a
rise in progesterone. These results suggested that the
breeding season commences with an increase in tonic
LH secretion which initiates the sequence of preovulatory
events leading to the first LH surge and that these
changes in LH secretion pattern occur rapidly within
less than a week. According to the authors, the transient
increments in progesterone may represent short
luteal phases which result from ovulation of immature
follicles. Finally, I’Anson and Legan (1988) suggested
that before the first oestrous cycle, a transition period
of 1–4 weeks exists, during which one or more increases
in LH pulse frequency and progesterone concentrations
may occur.
5.2.4. Current model of the photoperiodic control
of reproduction
It seems clear that the start of seasonal anoestrous
condition in the ewe results from the interruption of
the preovulatory sequence of events leading up to ovulation.
In order to detect in which step the sequence is
interrupted, Legan and Karsch (1979) studied all the
progression of events, beginning with the LH surge
and working back. Following various considerations,
they suggested that the primary cause of seasonal
anoestrus is not failure of the LH surge, behavioural
oestrus or absence of oestradiol rise or any mechanism
associated with these events. These considerations
have later received much support and it is now well
known that all preovulatory events and ovulation can
be induced in seasonally anovular ewes if they are
treated with multiple injections of GnRH (McLeod
et al., 1982; Southee et al., 1988). This leaves only
the first step in the sequence of events leading up to
ovulation—the sustained increase in basal LH secretion
(or GnRH, as this hormone dictates the secretion
of LH). A necessary condition for this hypothesis to
be correct (i.e. the disruption of a sustained increase
in basal LH secretion to be the responsible for the
establishment of seasonal anoestrous) is that a sustained
48 h increase in tonic LH secretion should not
be observed in three situations: firstly, following the
brief episodes of elevated LH levels during anoestrus,
secondly, following a treatment of progesterone in
the anoestrous season and thirdly, following the regression
of the last CL of the breeding season. All
these premises have been confirmed as reported above
in this section. The question that naturally arises at
this point is what prevents the sustained preovulatory
increase in LH secretion during anoestrus.
The clue to answer this question was first provided
by the observation that during the breeding season,
each preovulatory rise of oestradiol was accompanied
by a sustained parallel increase in LH while in
anoestrus an induced oestradiol rise was accompanied
by a pronounced drop in LH levels (Legan and Karsch,
1979). These opposite actions of oestradiol would suggest
that in the anoestrous season this steroid exerts a
strong negative feedback effect on LH secretion. Probably
the first convincing evidence that there is a seasonal
shift in the ability of oestradiol to inhibit LH
secretion was provided by the work of Legan et al.
(1977). In their study, in which a group of ovariectomised
ewes were treated with oestradiol implants,
a marked seasonal change in circulating LH was observed.
During the breeding season, LH was elevated
but in anoestrus the level of this hormone was undetectable.
On the contrary, in the control group (ovariectomised
ewes without implants) no major seasonal
variation was detected, with the LH concentration being
elevated and maintained at levels similar to those
of the reproductive season in oestradiol treated ewes.
This study also showed a coincidence between the periods
of changes in LH response to oestradiol (2–3
weeks) and the periods of transition between breeding
and anoestrous seasons in intact ewes.
The considerations presented above, together with
the proven fact that the response of LH secretion to
oestradiol is controlled by photoperiod (Legan and
Karsch, 1980), led Karsch et al. (1980) to formulate an
hypothesis for the photoneuroendocrine control of seasonal
breeding in the ewe. According to this hypothesis,
during the breeding season the responsiveness of
the neuroendocrine system to the oestradiol negative
feedback is low and consequently, following the regression
of each CL, all the preovulatory events can
occur. During transition to anoestrus, the response to
oestradiol inhibition of LH starts increasing and when
the last CL of the breeding season regresses, tonic LH
secretion begins to increase but this increase is not sustained
because the accompanying onset of oestradiol
rise prevents it. In the absence of a suitable stimulus,
oestradiol would not reach the threshold necessary to
switch to positive feedback over LH, and as a consequence
LH surge and ovulation does not occur. At the
end of anoestrus, as the responsiveness to oestradiol
negative feedback diminishes, the sustained increases
in LH and oestradiol become possible again, thus enabling
oestradiol to reach the threshold for eliciting
the preovulatory LH surge allowing oestrous cyclicity
to be re-established.
The described hypothetical model for the control of
seasonal breeding in the ewe only took into account
the seasonal change in the ability of the LH pulse
generating system to become more or less sensitive
to the negative feedback effect of oestradiol, indicating
a photoperiodic-induced variation of this mechanism.
There is, however, evidence that photoperiod
also has a direct effect on the LH pulse generator,
independently of the action of steroids. This effect
has been observed in castrated rams kept under controlled
photoperiod (Pelletier and Ortavant, 1975) and
in long-term ovariectomised, not oestradiol treated
ewes, exposed to the annual cycle of natural photoperiod
(Goodman et al., 1982; Robinson et al., 1985a;
Thomas et al., 1988) or submitted to artificial controlled
photoperiods (Robinson, 1983). In all cases,
LH pulse frequency increased as days became shorter
and declined as day length increased.
Although the relationship between these two effects
and its importance remains to be established, the overall
perception collected from the literature is that quantitatively
the oestradiol feedback mechanism seems to
account for much of the reduction in LH pulse frequency.
Giving more support for this view, Karsch
et al. (1993) were unable to find a significant seasonal
difference in the frequency of both GnRH and LH pulsatility
in ovariectomised ewes not treated with oestradiol
(although trends for a reduced rate in anoestrus
were apparent) while oestradiol implants produced a
profound suppression of the frequency of these hormones.
Similar results for GnRH secretion were obtained
by Karsch et al. (1987).
The current model for photoperiodic control of ovarian
cyclicity was enunciated by Karsch et al. (1984)
and is very much based on the described model proposed
by Karsch et al. (1980) but in which the effect
of the direct photoperiod drive was incorporated. In
short, it suggests that under the inductive influence of
short days of the breeding season, there is a high drive
to the LH pulse generator eliciting high frequency of
GnRH discharges from the hypothalamus and in addition,
under such photoperiod, the negative feedback
effect of oestradiol is not strong enough to suppress LH
release. Therefore, the frequency of LH pulses can increase
sufficiently for the accomplishment of the preovulatory
sequence and ovulation occurs. Under the
inhibitory influence of long days in the anoestrous season
there is a low drive to the LH pulse generator and
additionally the pulse generator becomes very sensitive
to the negative feedback action of oestradiol. Consequently,
the low pulsatility of LH does not provide
sufficient stimulation to support a sustained oestradiol
increase and the preovulatory sequence cannot take
place as a result the oestrous cyclicity is arrested.
It is now well established that the negative feedback
action of oestradiol on LH secretion is brought about
via a reduction in the GnRH pulse secretion rather
than a major diminution of pituitary responsiveness
to GnRH (Karsch et al., 1987, 1993; Barrell et al.,
1992). The mechanisms by which changes in environmental
photoperiod induce different responses of
the GnRH neurosecretory system to the same pattern
of oestradiol secretion remains to be elucidated. An
important point to stress is that the GnRH neurones
in sheep (Lehman and Karsch, 1993; Herbison et al.,
1993; Herbison, 1995), as well as in other mammals
(Shivers et al., 1983; Herbison, 1995), do not seem
to have steroid receptors which add more complexity
to this matter. However, it is known that there are
many afferents to GnRH neurones which have the potential
to receive and transmit steroidal feedback signals
(Tilbrook and Clarke, 2001). In this regard, it has
been suggested that the response to oestradiol negative
feedback that leads to anoestrus involve afferents
from other neurones (Xiong et al., 1997; Lehman
et al., 1997). This fact could lead to the speculation
that seasonality is not due to changes in GnRH neurones
but rather to changes in afferent neurones which
regulate GnRH neurosecretion. However, this is probably
not entirely the case, and some action may be
reserved to the GnRH neurones, since the study of
Xiong et al. (1997) has shown evidence that seasonality
may induce morphological changes in GnRH cell
bodies.
As the most seasonal hormonal variation occurs in
prolactin concentration, with highest levels coinciding
with long days and lowest levels coinciding with
short days (Kennaway et al., 1987), and since high
prolactin levels are normally associated with ovarian
inactivity, it has been suggested that the seasonally
high prolactin concentration may be responsible for
the seasonal impairment of reproductive function in
the sheep (Walton et al., 1977, 1980). However there
is little evidence for such a role of prolactin. Experiments
carried out both in the ram and in the ewe in
which manipulation of photoperiod have been used to
dissociate the pattern of prolactin secretion from seasonal
reproductive changes have shown that regression
of the testes still occur when rams have low levels
of prolactin (Almeida and Lincoln, 1984), and ewes
show oestrous cyclicity at times when prolactin concentrations
are high (Worthy et al., 1985; Jackson and
Jansen, 1991). Detailed information about the seasonal
prolactin secretion and its role in seasonal reproduction
in sheep and other mammals is provided by the
review of Curlewis (1992).
5.3. Transfer of photoperiodic information to the
hypothalamo–pituitary axis
From the discussion presented in the previous section,
it is clear that the seasonality of reproductive
activity in sheep is primarily due to changes in the responsiveness
of the GnRH neurosecretory system to
the negative feedback action of oestradiol, which in
turn are dictated by variations in length of the daily
photoperiod. The next sections are intended to review
the way by which photic information from the environment
is received, transmitted and measured throughout
the neuroendocrine system and the role played by
photoperiod in timing the beginning and the end of
the breeding season.
5.3.1. Anatomical pathway
The photoneuroendocrine pathway whereby photic
cues are picked up and relayed to the GnRH generating
system has been extensively investigated and
is now well understood (Legan and Winans, 1981;
Karsch, 1984; Karsch et al., 1984; Turek et al., 1984;
Hansen, 1985; Lincoln, 1992). Based on evidence obtained
mostly in hamsters, Legan and Winans (1981)
first proposed the current model for the pathway in
sheep which since then has received much additional
experimental support. According to this model, the
photic stimuli are first received by the retina which
contains the photoreceptors necessary for the photoperiodic
control of reproduction in this species. The
photic information is then transmitted from these receptors
to the suprachiasmatic nuclei (SCN) of the
hypothalamus via a monosynaptic tract known as the
retinohypothalamic tract. The SCN functions as an internal
biological clock regulating endogenous circadian
rhythms. After receiving input from the circadian
system, the photoperiodic message is transmitted to
the pineal gland by way of its sympathetic innervation
designated by superior cervical ganglia (SCG).
The pineal gland functions as a transducer converting
neural information regarding the light-dark cycle
into a hormonal signal which take the form of a circadian
rhythm of melatonin secretion. The pattern of
this melatonin signal, which can be interpreted as inductive
or suppressive, sets the frequency of the LH
pulse generating system and determines its capacity
to respond to the negative feedback action of oestradiol
(Lincoln, 1992; Williams and Helliwell, 1993;
Malpaux et al., 1996).
Experimental evidence for the existence and functioning
of the described retinohypothalamic tract has
been provided by various studies, based mainly in the
destruction of its components, which have shown that
the interruption of this pathway renders the animals
unresponsive to changes in day length and interferes
with the secretion of melatonin. Legan and Karsch
(1983) and Karsch et al. (1984) found that the photoperiodic
control was lost in ewes following blinding,
demonstrating the role of the photoreceptors located
in the eyes. A monosynaptic tract, independent of the
primary optic tract used for visual image perception,
linking the retina to the SCN, previously identified in
other species, has also been found in sheep by Legan
and Winans (1981) using a technique involving the
autoradiographic localisation of [3H] proline. The implication
of the SCN has been shown by Przekop and
Domanski (1980), Jackson et al. (1986) and more recently
by Scott et al. (1995) after confirmation that
the ewes would not respond to day length changes
following the lesion of this section of the brain. Both
the removal of the superior cervical ganglionectomy
(SCG) or the pineal gland resulted in an inability of
rams (Lincoln, 1979; Lincoln et al., 1989) and ewes
(Bittman and Karsch, 1984) to respond to changes in
photoperiod, confirming the indispensability of those
anatomic structures.
5.3.2. The role of melatonin
Melatonin is the main hormone secreted by the
pineal gland and is by far the most extensively studied
pineal compound. In several species, melatonin
can also be synthesised in other organs such as the
retina, intestine and salivary glands (Vivien-Roels and
Pévet, 1983) but in most mammals the pineal gland
accounts for almost all the melatonin in circulation
(Yellon et al., 1992). Numerous studies have provided
evidence that the pattern of secretion of this hormone
follows a circadian rhythm with significant secretion
occurring only during the dark period of the day with
the light acting as a supressor. Consequently, melatonin
levels in both the pineal gland and the blood are
high at night and low during the day. There is also
experimental evidence to show that exposure of animals
to light at night readily suppresses the secretion
of melatonin (Lincoln, 1992). The question of
which parameter of the nightly melatonin secretion
is used to measure the day length (i. e. amplitude,
duration or phase relative to the 24 h light/dark period)
has been extensively discussed in the literature.
From the two major hypotheses that have emerged, the
“phase hypothesis” and the “duration hypothesis”, it
seems that the most convincing evidence to date supports
the “duration hypothesis” because sheep have
been shown to respond to the melatonin signal irrespective
of when it is received during the 24 h period
(Wayne et al., 1988). Therefore, the duration of nocturnal
elevation in melatonin level may constitute the
message whereby the pineal mediates the photoperiodic
regulation of hormonal secretion. Long days are
characterised by a short duration of melatonin secretion
while short days are characterised by a longer
duration of secretion. However, the circadian rhythm
persists in constant darkness, being eliminated in constant
light (Rollag and Niswender, 1976) or when
animals are submitted to pinealectomy or superior cervical
ganglionectomy when melatonin is secreted in
small or undetectable amounts (see Deveson et al.,
1992 for review). This indicates that the rhythm is
generated endogenously, presumably under the control
of the SCN. The definitive demonstration that melatonin
influences the reproductive seasonality in sheep
came from studies in which melatonin was infused
into pinealectomised ewes in patterns mimicking long
and short days and it was found that the reproductive
response was similar to pineal-intact ewes experiencing
those photoperiods (Bittman and Karsch, 1984;
Karsch et al., 1984; Bittman et al., 1985).
The major question being addressed at this stage
of the discussion relates to the way by which the
melatonin secretion pattern operates to change the
sensitivity of the GnRH pulse generator to the oestradiol
negative feedback. The sites and mechanisms of
action of melatonin have been extensively studied and
reviewed in the literature (Kennaway and Hugel, 1992;
Williams and Helliwell, 1993; Kennaway and Rowe,
1995; Malpaux et al., 1996; Goldman, 2001) and yet
there is still no clear indication of where and how
melatonin acts. Although melatonin may act at different
levels of the reproductive system, the main action
may be within the central nervous system. Indeed,
a direct effect of melatonin on GnRH secretion was
demonstrated by Viguié et al. (1995) who observed
an increase in GnRH pulse frequency when ovariectomised
oestradiol treated ewes exposed to long days
received melatonin implants. The rise in GnRH pulse
frequency occurred simultaneously with an increase in
LH pulsatility 40–60 days after the beginning of melatonin
treatment. However, according to Malpaux et al.
(1996), a direct action of melatonin on GnRH neurones
appears unlikely. One reason is because most of
the GnRH neurones are located in the preoptic area
(POA) of the hypothalamus which does not seem to be
a site of action of melatonin and very few are located
in the mediobasal hypothalamus (MBH) which is a
putative site of action of this hormone. Also, the long
delay in the GnRH and LH responses to the melatonin
treatment suggests a more complex mechanism
and several neurotransmitters have already been implicated
in the process, such as dopamine, serotonin
and excitatory amino acids (glutamate, aspartate, etc.)
(Malpaux et al., 1996). The detection of the physiological
sites of action of melatonin has been attempted
using melatonin microimplants inserted into regions
of the hypothalamo–hypophisial complex which limits
the delivery of this hormone to those sites, in animals
maintained in a photoperiod of long days. Results
from this sort of study have shown that microimplants
positioned in the premammilary hypothalamic area
(PMH) (Malpaux et al., 1998) and in the MBH but
not in the POA induced an increase in LH secretion in
ewes (Malpaux et al., 1993) and an increase in FSH
secretion and testicular size in rams (Lincoln and
Maeda, 1992). On the other hand, several studies have
shown that the sheep pars tuberalis (PT) is also an
important site of melatonin action (De Reviers et al.,
1989; Morgan et al., 1989; Bittman andWeaver, 1990;
Stankov et al., 1991) but it is not clear whether this
is a crucial target for reproductive action. In fact,
while Lincoln (1994) reported that the administration
of melatonin in the PT affected the photoperiodically
induced cycles of FSH and prolactin secretion
in rams, other authors (Malpaux et al., 1994, 1995,
1998; Goldman, 2001) argue that melatonin in this
site only regulates the seasonal variation in prolactin
secretion and not the secretion of gonadotropins. But
whatever the mechanism and site of action of melatonin,
its administration either by daily dosing or
through constant-release devices allows short days to
be mimicked and therefore it can be used to control
the seasonal reproduction in both the ram and the ewe.
However, for the treatment to be effective the animals
have to have pre-experienced a period of exposure to
long days just before receiving the melatonin and the
response takes 2–3 weeks in the ram (Chemineau et al.,
1992) and 40–60 days in the ewe (Haresign, 1992;
Viguié et al., 1995) to be achieved.
Considering the fact that there are breed differences
in the reproductive response of sheep to changes in
photoperiod and that seasonal reproduction is driven
by the pattern of melatonin secretion, it could be expected
that breed differences would be due to different
genetic abilities to secrete melatonin. However this
does not seem to be the case since Lincoln et al. (1990)
report examples in which the same pattern of melatonin
secretion (i.e. the duration of the period of elevated
levels reflects the period of darkness) is found
among breeds which differ in the degree of seasonality
of reproduction. Therefore, it may not be the melatonin
signal which differs between breeds but the way
the signal is translated in the brain.
5.4. Regulation of the annual reproductive cycle
First of all, it is important to stress the existence in
the sheep of an endogenous circannual rhythm of reproductive
neuroendocrine function which means that
seasonality persists in the absence of photoperiodic information.
Evidence for such endogenous rhythmicity
is provided by the fact that long term changes in reproductive
condition continue to be expressed during
prolonged exposure of animals to a constant day length
(Howles et al., 1982; Karsch et al., 1989; Jackson and
Kao, 1990), or following procedures that functionally
block the transmission of photoperiodic information
to the GnRH pulse generating system such as surgical
blinding (Legan and Karsch, 1983), pinealectomy
(Barrell and Lapwood, 1979; Kennaway et al.,
1984; Lincoln et al., 1989) or superior cervical ganglionectomy
(Lincoln et al., 1989). However, the reproductive
shifts are neither synchronised among animals
nor in phase with the natural breeding cycle.
In this context, the prevailing current view is that the
seasonal reproduction in sheep is generated by an endogenous
circannual rhythm of reproductive neuroendocrine
activity and that the role of photoperiod is
to synchronise but not to create this rhythm (Karsch
et al., 1989; Malpaux et al., 1989; Woodfill et al.,
1994; Barrell et al., 2000). The mechanism by which
photoperiod synchronises the rhythm is not yet well
understood. However, it seems that not all photoperiodic
information of the year is required for animals
to synchronise the rhythm and that not all portions of
the annual photoperiodic cycle are equally effective
at synchronising it. Woodfill et al. (1991) found that
pinealectomised ewes exhibited synchronous annual
reproductive cycles when treated with only a 70-day
block of a long-day pattern of melatonin each 365
days. Malpaux et al. (1989) reported findings which
led them to conclude that it is the time at which increasing
photoperiod is first experienced in late winter
or spring that determines when the subsequent breeding
season begins. In one of their experiments in which
ewes were exposed to increases in day length at different
time-intervals after the winter solstice, these workers
found that when ewes perceived long days earlier
than normal, the breeding season was advanced.
In contrast, when ewes perceived long days later, the
breeding season was delayed. These authors concluded
that long days play a critical role in positioning the
breeding season to the autumn. All these results were
confirmed by the study of Woodfill et al. (1994) who
found that the annual rhythm can effectively be synchronised
with a period of 90 days of long-day photoperiodic
cues (summer melatonin pattern) perceived
around the summer solstice. During winter, the melatonin
pattern secreted at that time fails to synchronise
the rhythm. Recently, the work of Barrell et al. (2000)
demonstrated the inability of the winter melatonin pattern
to entrain the rhythm also during the summer
stage of the rhythm. These findings indicate that the
mere presence of a circadian melatonin pattern is insufficient
for rhythm entertainment. What really determines
entrainment seems to be the characteristics
of the pattern, particularly the pattern that mimics the
photoperiodic signals of summer. Adding to this, the
findings that the summer pattern applied during winter
(Woodfill et al., 1991) or at random stages of the
free-running rhythm (Woodfill et al., 1992) synchronises
the rhythm, finally allows the inference that the
synchronisation of the circannual reproductive rhythm
of sheep is dependent on the quality of the photoperiodic
signal (i.e. the summer photoperiodic signal) and
not on the rhythm stage.
5.5. Photorefractoriness
Under natural conditions, sheep breed during the
autumn when the increasing duration of the melatonin
signal appears to be stimulatory to reproductive activity.
However, ewes maintained on stimulatory short
days eventually cease breeding activity (Robinson and
Karsch, 1984; Minton, 1990). Conversely, ewes kept
on long day lengths which are considered to be inhibitory
to reproduction become reproductively active
after some time (Worthy et al., 1985; Robinson et al.,
1985b). The rams also perform in a similar way and
if left in the natural annual photoperiodic cycle, the
LH and testosterone blood levels as well as the testicular
weight start increasing generally before the summer
solstice (Pelletier and Almeida, 1987) when day
length is still increasing and therefore not stimulating
for reproductive activity. On the other hand, in
natural conditions, the same photoperiod occurs twice
a year in a symmetric fashion in relation to the solstices.
However, sheep are reproductively stimulated
at one time of the year but inhibited under the same
photoperiod at the other. The preceding considerations
provide evidence that the timing of onset and cessation
of the reproductive season is not regulated by an
absolute critical day length, rather it is highly dictated
by the recent photoperiodic history experienced
by the animal. The assumption of this phenomenon
led to the emergence of the concept of photorefractoriness.
According to this concept, if an animal is exposed
to a fixed photoperiod for a prolonged period
(in sheep, 30–32 weeks for gradual shifts under natural
conditions or 16–18 weeks for artificial abrupt
shifts, Nicholls et al., 1989) it loses the reproductive
response to that photoperiod and it is said to be photorefractory
(Robinson and Karsch, 1987; Williams
and Helliwell, 1993). Sheep can be refractory to either
long or short days. In this view, and according
to Malpaux et al. (1989) and Minton (1990) the onset
of anoestrous in ewes in late winter/early spring is
not brought on by the arrival of long days; rather the
ewes cease reproductive activity because they become
insensitive to stimulatory short days. Similarly, ewes
start ovulating in late summer/early autumn not because
of the exposure to short days but because they
are no longer inhibited by long days. Since the transition
from anoestrus to breeding season does not require
a decrease in day length and because reductions
in photoperiod prolong the period of reproductive activity
(Malpaux et al., 1988a, 1989; Nicholls et al.,
1989; Malpaux and Karsch, 1990) it has been suggested
that in natural conditions the role of long days is
to synchronise the onset of the breeding season while
short days play the determining role in sustaining it
(Malpaux et al., 1989; Malpaux and Karsch, 1990).
It has been shown that the lack of response to a fixed
photoperiod is not due to a change in the circadian
pattern of melatonin secretion (Karsch et al., 1986;
Malpaux et al., 1987, 1988b) and therefore it may be
caused by a change in the response of the endocrine
system to the melatonin signal as was first suggested
in the case of hamsters by Bittman (1978) and later in
sheep by Karsch et al. (1986).
5.6. The role of thyroid hormones in seasonal
reproduction
Thyroid hormones play an important role for reproductive
seasonality in a large range of species including
birds, rodents and mammals. The first evidence
of the involvement of these hormones in seasonal reproduction
of sheep was provided by Nicholls et al.
(1989) who found that ewes thyroidectomised in late
anoestrous season entered normally into the breeding
season but continued to exhibit regular oestrous cycles
throughout the following anoestrous season, remaining
in this condition for more than 1 year. It is now
well known that thyroid hormones do not influence
transition into the breeding season but their presence is
required for its termination. Therefore, in the absence
of these hormones the seasonal reproductive rhythm
is not expressed. The site and mechanism of action
of thyroid hormones remain to be elucidated but according
to Karsch et al. (1995) it may act within the
brain to promote morphological changes in the GnRH
neurosecretory system. Therefore, the way in which
the thyroidectomy prevents the effect of season on reproduction
does not appear to be due to an altered
metabolism of steroid hormones, to a disruption of all
seasonal processes or to a disturbance of the pathway
responsible for the transduction of the photoperiodic
stimuli. Rather, the effect of thyroidectomy seems to
be more specific, being restricted to the seasonal increase
of the oestradiol negative feedback on GnRH
release (Dahl et al., 1994, 1995). More detailed information
on the involvement of thyroid hormones in
seasonal reproduction is provided by the reviews of
Karsch et al. (1995) and Gerlach and Aurich (2000).
The seasonal reproduction and the endocrine
mechanisms involved can largely be influenced by
behavioural stimuli released through the social relationships
that an animal (both the ram and the ewe)
establishes with others of the same species. This important
aspect of the reproductive process in sheep
was recently reviewed by Rosa and Bryant (2002).
6. Conclusion
Seasonality of the reproductive activity in sheep is a
general phenomenon for mid and high-latitude breeds.
The seasonal variations in mating concern both males
and females. However, variations in gonadal activity
and sexual behaviour are less pronounced in the
ram than in the ewe. While in rams spermatogenesis
and sexual activity never stop, in ewes ovulation and
oestrus is arrested during variable periods. The daily
photoperiod has long been identified as the determinant
factor of seasonal breeding while environmental
temperature, nutrition, behaviour, lambing date and
lactation period exerts a modulator effect. The central
aspect of the current model of the photoperiodic
control of seasonality is that under the influence of
long days in the anoestrous season the LH pulse generating
system becomes very sensitive to the negative
feedback action of steroids. The mechanisms involved
are complex and not entirely understood. Melatonin,
through its duration of nocturnal secretion, is the hormone
responsible for the translation of the day length
information to the reproductive axis by changing the
sensitivity of the GnRH pulse generator with consequent
modification on the pulsatile secretion of LH.
The exact site of action of melatonin within the central
nervous system is still controversial and requires
further research. Studies using melatonin microimplants
have indicated that the premammilary and the
mediobasal but not the preoptic areas of the hypothalamus
are physiological sites of action of melatonin
involved in the control of seasonal reproduction. The
pars tuberalis, even though having been recognised as
an important site of melatonin action, is not consensually
considered as being a crucial target for reproductive
action.
Photoperiod is responsible for the synchronisation
of reproductive activity with the environment but not
for the generation of a circannual reproductive rhythm.
In fact an endogenous rhythm exists in the absence of
any photic stimulus and therefore the role of photoperiod
is to synchronise but not to create this rhythm. It
has recently been demonstrated that not all photoperiodic
information of the year is required for animals
to synchronise the rhythm and that not all portions of
the annual photoperiodic cycle are effective at synchronising
it. The winter pattern of melatonin secretion
fails to synchronise the rhythm at any time of the
year. On the other hand the summer melatonin pattern
is effective at synchronising during the summer and
indications are that it is also effective in any other period
of the year. However this subject requires further
investigation.
Finally, it should be considered that the thyroid hormones
also have an important role in seasonal reproduction
but the site, the mechanisms of action and
its integration in the current neuroendocrine model of
photoperiodic control of seasonal reproduction need
to be elucidated.
Acknowledgements
The authors would like to thank PRAXIS XXI programme,
Lisbon, for financial support.
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