A . Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
9
expenditure mice: Pelleymonter et al., 1995. Plas- ma levels of leptin seem to be lower in feed-re-
stricted than in control gilts Prunier and Quesnel, unpublished data. Therefore, leptin may be involved
in the effects of nutrition on reproduction, at least as a regulator of the nutritional status. Direct effects of
leptin at the hypothalamic–pituitary level could also play a role since RNA messengers coding for the
long-form leptin receptor have been detected in hypothalamic and anterior pituitary tissues of ewes
and since this expression in the ventromedial and arcuate nuclei of the hypothalamus is higher in
feed-restricted than in well-fed ewes Dyer et al., 1997. Moreover, leptin exhibits a high potency to
Fig. 4. Influence of daily feed intake high vs. low: 300 vs. 80
increase FSH and LH release from male rat
of the energy requirements for maintenance from luteolysis
hemipituitaries incubated in vitro, and to stimulate
induced by a prostaglandin analogue, alfaprostol on plasma
GnRH secretion from medio-basal hypothalamus
concentrations of progesterone in gilts adapted from Prunier et
explants Yu et al., 1997. Finally, leptin is able to
al., 1999.
stimulate LH secretion in vivo in mice and female rats subcutaneous injections: Ahima et al., 1996;
intracerebroventricular injections: Yu et al., 1997. metabolic clearance of oestradiol-17b may be de-
creased by feed restriction and influence LH secre- 3.3.5. Metabolic clearance of steroids
tion. However, growth and steroid secretion of the It has been demonstrated that hepatic portal blood
oestrogenic follicles are under the control of gona- flow and metabolic clearance rate of progesterone are
dotrophins see Section 2.2 whose release is in- decreased in ovariectomized gilts submitted to feed
hibited during feed restriction. Therefore, peripheral restriction Prime and Symonds, 1993. Moreover,
concentrations of oestradiol may not be increased lower concentrations of progesterone have been
and could even be decreased during feed restriction. observed in well-fed than in feed-restricted gilts at
Such a hypothesis is supported by the observation of the beginning of gestation Dyck et al., 1980; Dyck
lower concentrations of oestradiol-17b in restricted- and Kennedy, 1995; Jindal et al., 1996. Therefore,
fed than in full-fed gilts at 23 and 53 h after we have investigated in gilts whether plasma con-
induction of luteolysis by alfaprostol Prunier et al., centrations of progesterone around luteolysis could
1999. Similarly, concentrations of oestradiol-17b be modified by the level of feeding Prunier et al.,
were low in follicular fluid of oestrogen-active 1999. Regression of the corpora lutea was induced
follicles Spicer et al., 1991 and in plasma Rhodes at the end of the luteal phase by an injection of a
et al., 1996 of restricted-fed compared with well-fed prostaglandin-F a analogue alfaprostol. From the
heifers.
2
time of the alfaprostol injection, gilts received either 80 or 300 of the maintenance energy requirements
for 3 days. Progesterone was significantly higher in
4. Main effects of nutrition on the ovaries
feed-restricted than in full-fed gilts from 5 to 53 h after the induction of luteolysis Fig. 4. Since
Nutrition may influence ovarian function through progesterone is known to inhibit LH pulsatility,
gonadotrophin-mediated effects as described previ- maintaining relatively high levels of this steroid in
ously but also through direct effects of nutrients underfed gilts around luteolysis may be detrimental
and or of metabolic hormones insulin, hormones for the recruitment and selection of preovulatory
from the somatotrophic axis, cortisol, thyroid hor- follicles. Similarly, it can be postulated that the
mones or even leptin.
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. Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
4.1. Influence of nutrition on folliculogenesis 4.1.2. Late steps of folliculogenesis
Cosgrove et al. 1992 have tried to evaluate the 4.1.1. Early steps of folliculogenesis
influence of feed restriction on large 2–6 mm but To our knowledge, there are only two reports
not preovulatory follicles. They have shown that relating the effects of nutrition to the development of
diameter, antral volume and oestradiol synthesis of small follicles 0.4–3 mm in diameter, one in
the largest follicles were reduced in feed-restricted prepubertal gilts Dufour et al., 1985 and the other
prepubertal gilts. These effects occurred despite in reproductive sows Quesnel et al., 1998a. In both
similar plasma concentrations of LH and FSH, studies, it was observed that feed restriction alters
suggesting that nutrition influences folliculogenesis, the repartitioning of healthy follicles between size
at least in part, through gonadotrophin-independent classes. For instance, it has been shown that the
mechanisms. proportion of 0.4–1.0 mm healthy follicles to the
Numerous researchers have determined the in- total number of antral follicles is increased whereas
fluence of feed restriction on ovulation rate. Data the proportion of 1.0–2.9 mm healthy follicles is
obtained in cyclic gilts show that starting feed decreased in feed-restricted lactating sows Fig. 5.
restriction during the luteal phase induces a reduction When oestrus occurs 4–7 days after weaning, pre-
in the number of corpora lutea at the subsequent ovulatory follicles are probably recruited immedi-
ovulation Table 4. In this situation, feed restriction ately after weaning in the 1.0–2.9 mm size class.
occurs at least during recruitment and selection of Therefore, it can be hypothesized that the relatively
the preovulatory follicles. In reproductive sows, most low number of follicles from this size observed in
researchers have determined the effects of feed level feed-restricted lactating sows may result in a delayed
during lactation on the ovulation rate after weaning. return to oestrus and or in a lower ovulation rate
Therefore, they have imposed the nutritional deficit after weaning. In fact, the resumption of follicular
before recruitment of the preovulatory follicles. In development 48 h after weaning is more variable in
this situation, feed restriction has no clear effect on feed-restricted than in control sows Quesnel et al.,
the ovulation rate whereas it delays the occurrence of 1998a.
oestrus in most studies Table 4. Similarly, King and Williams 1984b have shown a prolonged
weaning-to-oestrus interval but similar ovulation rates in primiparous sows submitted to protein
restriction during lactation. Few studies have evalu- ated the effects of feed intake around ovulation or
between weaning and oestrus 5 during recruitment and selection. Their results do not show any clear
effect of the level of feed intake on the ovulation rate Table 4.
4.2. Nutritional mediators 4.2.1. Insulin
Insulin is a good candidate for mediating the effects of nutrition on the ovaries. There is evidence
from in vitro studies that insulin stimulates uptake and utilization of nutrients and regulates growth and
proliferation of pig granulosa cells for review, see
Fig. 5. Average proportion of healthy antral follicles per size class
Booth, 1990. It also acts on differentiation, and
to the total number of antral follicles in lactating sows submitted
potentiates FSH-stimulated induction of LH recep-
to high or low levels of feeding adapted from Quesnel et al.,
tors as well as steroid production by pig granulosa
1998a. P , 0.05 between groups.
A . Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
11 Table 4
Influence of feed restriction during at least one part of the luteal phase and during the follicular phase or during oestrus or during lactation or between weaning and oestrus on the subsequent ovulation rate OR and, for weaned sows, on the weaning-to-oestrus interval WOI, days
a
Physiological stage Reference
Feed supply OR
WOI High
Low High
Low High
Low Cyclic gilts
Luteal and Cox et al., 1987
270 135
15.8 13.4
– –
follicular phases Flowers et al., 1989
270 135
16.0 9.4
– –
Beltranena et al., 1991 –
– 13.5
11.1 –
– Ashworth, 1991
380 90
19.2 14.2
– –
Oestrus Lodge and Hardy, 1968
– –
14.7 12.1
– –
Weaned sows Lactation
King and Williams, 1984a 85
40 14.4
13.4 7.6
19.9 Kirkwood et al., 1987
85 45
18.1 18.6
4.3 5.8
Kirkwood et al., 1990 80
40 17.6
17.7 6.0
8.9 Baidoo et al., 1992b
80 45
16.2 16.7
5.9 7.5
Zak et al., 1997 80
45 19.9
15.4 3.7
5.6 Quesnel and Prunier, 1998
90 60
19.2 20.7
5.7 5.9
Zak et al., 1998 85
50 14.4
15.6 4.2
6.3 After weaning
Den Hartog and van der Steen, 1981 –
– 15.2
14.8 9.1
8.2 King and Williams, 1984a
285 115
14.6 13.2
13.4 14.1
Baidoo et al., 1992b 245
155 16.6
16.2 6.0
5.9
a
Feed supply is the estimated ratio between metabolic energy intake and requirements for maintenance in prepubertal, mature and pregnant gilts, and weaned sows or for maintenance 1 milk production in lactating sows. When this ratio was not indicated in the
publication, it was calculated in the same way as for Table 2. P , 0.05 between control and feed-restricted groups, within criteria.
cells May and Schomberg, 1981. Some results 4.2.2. Hormones from the somatotrophic axis
from in vivo studies also suggest that insulin stimu- In the pig, as in other species, growth hormone
lates folliculogenesis directly at the ovarian level: for GH secretion by the pituitary as well as insulin-like
example, Cox et al. 1987 have shown that insulin growth factor-I IGF-I secretion by the liver are
treatment starting in the early follicular phase in- under metabolic influences for reviews, see Breier
creases the ovulation rate without a clear effect on and Gluckman, 1991; Thissen et al., 1994. Under-
plasma LH. However, insulin treatment may have no nutrition leads to a rise in circulating GH, to a
influence insulin treatment in lactating sows: Ques- decrease in liver response to GH decreased GH
nel and Prunier, 1998; insulin treatment during the binding or a post-receptor defect, to a decrease in
follicular phase of cyclic gilts: Quesnel, Jan and circulating IGF-I and to changes in binding proteins
Prunier, unpublished data or have a negative in- BPs for the IGFs. In numerous studies designed to
fluence insulin treatment between weaning and determine the influence of feed level on ovarian
oestrus: Rojkittikuhn et al., 1993b on ovulation rate. activity in the female pig, low concentrations of
Therefore, we can conclude that insulin has a IGF-I in plasma and or in follicular fluid have been
positive influence on nutrition, growth and develop- associated with reduced ovulation rate or impaired
ment of follicular cells, but direct evidence is still folliculogenesis Cosgrove et al., 1992; Charlton et
missing to demonstrate that a decrease in insulin al., 1993; Booth et al., 1994; Quesnel et al.,
secretion due to feed restriction is responsible, even 1998a,b. In vitro studies have shown that IGF-I
in part, for lower ovulation rate or delayed ovulation and or GH stimulate mitogenesis and amplify the
in female pigs. effects of FSH on the induction of LH receptors and
12 A
. Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
on steroidogenesis by granulosa cells for review, see 4.2.4. Metabolic clearance of steroids
Booth, 1990. In vivo manipulation of GH levels has Higher concentrations of progesterone in feed-
led to contradictory results. For example, treatment restricted females see Section 3.3 may influence
of cyclic gilts with exogenous GH may induce folliculogenesis directly at the ovarian level since
anoestrus or increase the ovulation rate Kirkwood et progesterone inhibits preovulatory growth of the
al., 1988, 1989. GH implants have positive effects follicles see Section 2.2. Indeed, we have recently
on the number of medium-sized follicles 4–6.9 mm observed that plasma concentration of oestradiol
and on the concentration of IGF-I in plasma and after induced luteolysis was decreased in feed-re-
follicular fluids of prepubertal gilts Echternkamp et stricted gilts with high concentrations of progester-
al., 1994. Over expression of GH in transgenic one suggesting that preovulatory growth of the
females has a detrimental influence on the number of follicles was impaired Prunier et al., 1999.
oestrogenic follicles . 5 mm and on their ability to synthetize oestradiol before puberty Guthrie et al.,
1993. Therefore, hormones from the somatotrophic
5. Conclusion
