Livestock Production Science 63 2000 1–16 www.elsevier.com locate livprodsci
Review article
Nutritional influences on the hormonal control of reproduction in female pigs
A. Prunier , H. Quesnel
Station de Recherches Porcines , I.N.R.A., 35590 Saint-Gilles, France
Received 8 October 1998; received in revised form 14 April 1999; accepted 30 April 1999
Abstract
Effects of nutrition on age at puberty, return to oestrus after weaning, ovulation rate and embryo survival have been observed in the pig. Nutrition may influence reproduction at the three levels of the hypothalamic–pituitary–ovarian axis via
neuroendocrine pathways and or variation in metabolic clearance of reproductive hormones. For instance, undernutrition impairs the gonadotrophin-releasing hormone GnRH pulse generator while refeeding restores luteinizing hormone LH
secretion. Nutrition influences follicular growth and maturation; for example, the percentage of small 1–3 mm healthy follicles and the ovulation rate are decreased under feed restriction. Detection of hormone receptors in tissues and both in
vitro and in vivo studies suggest that insulin, cortisol, thyroid hormones and hormones from the somatotrophic axis could be mediators of the effects of nutrition on reproduction. These hormones are able to alter folliculogenesis directly at the ovarian
level as either hormones controlling nutrition of the cells, growth factors insulin and insulin-like growth factor-I or amplifiers of the action of the gonadotrophins. Insulin and cortisol, at least, may influence gonadotrophin secretion through
action at the hypothalamic–pituitary level. Decreased metabolic clearance of progesterone resulting in increased plasma concentrations of this hormone could be involved in the inhibition of gonadotrophin release and reduction of the ovulation
rate occurring in feed-restricted cyclic gilts.
2000 Elsevier Science B.V. All rights reserved.
Keywords : Reproduction; Pig; Gonadotrophin; Ovarian follicle; Metabolic status
1. Introduction voluntary feed intake of sows is generally insuffi-
cient to meet their nutrient requirements Noblet et Peripubertal gilts are often submitted to stressful
al., 1990. This risk of nutrient deficit is particularly conditions transportation, vaccination, mixing with
acute in young sows which have lower appetite than unfamiliar animals, etc. which may have marked
multiparous sows despite similar milk production negative effects on their appetite. During lactation,
Dourmad, 1988. The nutrient deficit may increase in subsequent years for sows of all parities if the
current trend for improving prolificacy is maintained. Indeed, both milk production and appetite increase
Corresponding author. Tel.: 1 33--9928-5056; fax: 1 33-2-
with litter size but the augmentation of feed intake is
9928-5080. E-mail address
: prunierst-gilles.rennes.inra.fr A. Prunier
not sufficient to compensate for nutrient require-
0301-6226 00 – see front matter
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2 A
. Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
ments O’Grady et al., 1985. Inadequate nutritional 2. Main characteristics of the hypothalamic–
intake may influence reproductive performance of pituitary–ovarian axis
female pigs in various ways: it may delay puberty attainment and return to oestrus after weaning,
2.1. Gonadotrophin secretion decrease ovulation rate and either reduce nutritional
inadequacy occurring before ovulation or improve Synthesis and release of luteinizing hormone LH
nutritional inadequacy occurring after ovulation by the pituitary cells are tightly controlled by
embryonic survival for reviews, see Den Hartog and gonadotrophin-releasing hormone GnRH of hypo-
van Kempen, 1980; Aherne and Kirkwood, 1985; thalamic origin Fig. 1. LH is secreted in a pulsatile
Kirkwood and Aherne, 1985; Dourmad et al., 1994; manner and each pulse of LH coincides with a pulse
Cosgrove and Foxcroft, 1996; Foxcroft, 1998. of GnRH for reviews, see Kraeling and Barb, 1990;
These effects of undernutrition on reproductive Foxcroft et al., 1994. Therefore, LH secretion is
efficiency of the female pig may be related to principally under the influence of factors acting on
physiological mechanisms acting at various points the GnRH neurons. These factors include numerous
along the hypothalamic–pituitary–ovarian–uterine neuropeptides endogenous opioids, serotonin, cat-
axis. They may be mediated by nutrients, hormones echolamines, neuropeptide Y, excitatory amino acids,
or neuropeptides primarily involved in the control of etc. from intra- and extra-hypothalamic origin which
nutritional function. In the present review, we briefly allow the animal to integrate influences from internal
describe the main characteristics of reproductive origin age, metabolic and health status, etc. and the
function before focussing on the endocrine mecha- external environment light, ambient temperature,
nisms that may explain the effects of nutrition on it. nutrient supply, social and physical environments,
Nutritional effects on embryonic survival, which etc..
have been reviewed recently Foxcroft, 1998, will Ovarian steroids exert feedback effects on the
not be discussed. hypothalamic–pituitary axis Fig. 1. Progesterone
Fig. 1. Main characteristics of the hypothalamic–pituitary–ovarian axis in female pigs.
A . Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
3
always has an inhibitory influence. Oestrogens and forming-growth factor or a negative follistatin
more particularly oestradiol-17b which are synthet- influence. Therefore, FSH is generally high when
ized by the follicles mainly exert negative effects on ovaries are quiescent during infancy in prepubertal
LH secretion. However, when concentrations are gilts: Camous et al., 1985 and decreases when antral
sufficiently high, oestradiol can act as a positive follicles become more numerous and differentiated
feedback signal to elicit the preovulatory LH surge. during the waiting phase in prepubertal gilts: Cam-
This level of oestradiol is attained during the follicu- ous et al., 1985; during the mid-follicular phase in
lar phase of the oestrous cycle when follicles are cyclic gilts: Prunier et al., 1987; Flowers et al.,
developed and differentiated enough to secrete high 1991.
amounts of oestrogens see Section 2.2.. As the central nervous system and the gonads
2.2. Folliculogenesis considerably influence the hypothalamic–pituitary
axis, frequency of the LH pulses varies between In prepubertal gilts, as well as in cyclic, pregnant,
physiological stages and between animals Table 1. lactating and weaned females, groups of primordial
For instance, LH pulsatility is 2-fold higher during follicles are continuously activated and start to
the early follicular phase than during the mid-luteal develop. Most of these growing follicles undergo
phase, increasing concomitantly with the decrease in atresia and only a minority less than 1 will
progesterone Flowers et al., 1991; Kemp et al., ovulate in cyclic females. An activated primordial
1998. Similarly, it jumps 2- to 3-fold shortly after follicle requires several months to reach the ovulat-
weaning Shaw and Foxcroft, 1985 due to the ory stage Morbeck et al., 1992. Growth until
removal of the suckling stimuli exerted by the piglets antrum formation diameter | 0.4 mm according to
for review, see Quesnel and Prunier, 1995. Quesnel et al., 1998a is very slow and due principal-
Follicle-stimulating hormone
FSH is
also ly to oocyte growth and to multiplication of sur-
synthetized and released by the pituitary, and is also rounding cells. Final growth from 1–4 mm to the
under the positive control of GnRH. However, ovulatory size 6–10 mm is very rapid and requires
patterns of variation of LH and FSH are very about 4–6 days Dailey et al., 1976; Morbeck et al.,
different in the female pig Camous et al., 1985. In 1992. This growth is due to cell proliferation
fact, FSH secretion is primarily controlled by the followed by a rapid increase in volume of the
inhibitory influence of inhibin from follicular origin antrum. It is accompanied by differentiation of
which acts directly at the pituitary level for review, follicular cells as evidenced by an increased secre-
see Foxcroft et al., 1994. Other ovarian peptides are tion of inhibin and oestradiol, and by appearance of
also probably involved in the regulation of FSH LH receptors on granulosa cells for review, see
secretion, having either a positive activin, trans- Foxcroft and Hunter, 1985.
Table 1
a
Comparison of LH pulsatility between physiological stages in female pigs Number of LH pulses 6 h
Prepubertal gilts Infancy | 1 month of age
Juvenile | 3 months of age 0.5–1
1.5–2.5 Cyclic gilts
Luteal phase Follicular phase
1–2 2.5–5
Sows Lactation
0–12 h after weaning 0.5–1.5
2–6
a
Adapted from Camous et al., 1985; Shaw and Foxcroft, 1985; Prunier et al., 1987; Flowers et al., 1991; Driancourt et al., 1995; Kemp et al., 1998; Zak et al., 1998.
4 A
. Prunier, H. Quesnel Livestock Production Science 63 2000 1 –16
Growth of the follicles up to 2–3 mm does not effect of nutrition on the hypothalamic–pituitary axis
require gonadotrophin support Driancourt et al., may have consequences on folliculogenesis and
¨ 1995; Brussow et al., 1996 but such growth seems
ovulation. to be controlled mainly by local ovarian factors such
as growth factors. Among healthy 1- to 4-mm 3.1. Influence of nutrition on circulating levels of
follicles present at luteolysis or at weaning, 15–25 gonadotrophins
are recruited and selected to undergo preovulatory growth and to ovulate 4–7 days later whereas the
3.1.1. Influence of feed restriction others become atretic. In the female pig, there is no
The effects of feed restriction on circulating levels clear evidence showing that the signal for recruit-
of LH and or FSH have been evaluated in numerous ment and selection of these follicles is an increase in
experiments involving premature and cyclic gilts, as FSH as has been proposed for numerous other
well as lactating and weaned sows Table 2. In mammalian species. Guthrie and Bolt 1990 and
these studies, control females are fed either ad Hunter et al. 1992 have not associated any vari-
libitum Kirkwood et al., 1987; Mullan et al., 1991; ation in gonadotrophin secretion with preovulatory
Cosgrove et al., 1992; Booth et al., 1994; Zak et al., growth and have suggested that, in cyclic gilts, the
1997, 1998 or close to ad libitum Flowers et al., decline in progesterone at luteolysis is the signal for
1989; Baidoo et al., 1992a; Prunier et al., 1993a,b; recruitment and selection. However, ovulation can be
Peltoniemi et al., 1997; Quesnel et al., 1998a,b, or induced during the luteal phase by exogenous gona-
receive 125–150 of the energy requirements for dotrophins showing that preovulatory growth may
maintenance Armstrong and Britt, 1987; Prunier and occur despite high levels of progesterone Caldwell
Peintre, unpublished data. In most studies, restricted et al., 1969. An increase in LH pulsatility around
females receive 10–65 of the control feed intake luteolysis van de Wiel et al., 1981; Flowers et al.,
which is below, equal or above energy requirements 1991; Kemp et al., 1998 or immediately after
for maintenance Table 2. In young females pre- weaning for review, see Quesnel and Prunier,
pubertal, mature and early pregnant gilts, growth is 1995, without any clear variation in FSH, has been
retarded Flowers et al., 1989; Prunier et al., 1993a; observed in numerous studies. Moreover, experi-
Peltoniemi et al., 1997 and may even be suppressed ments with gonadotrophin deprivation have shown
Armstrong and Britt, 1987; Cosgrove et al., 1992; that FSH is necessary to support follicular growth
Booth et al., 1994, 1996 by feed restriction. During beyond 2–3 mm and LH beyond 4 mm Driancourt
lactation, the level of feeding of restricted sows is ¨
et al., 1995; Brussow et al., 1996. Therefore, it can never sufficient to meet energy requirements for
be concluded that recruitment and selection of the maintenance plus milk production and feed intake of
preovulatory follicles can occur only when the control sows is also below requirements in most
equilibrium between stimulatory factors at least LH studies Table 2.
and FSH and inhibitory factors e.g. progesterone in Detailed analyses of the data show that LH
cyclic females or hormones induced by suckling in pulsatility is inhibited during the period of feed
lactating sows is displaced in favour of the stimulat- restriction in a majority of experiments regardless of
ory factors. As selected follicles develop, oestradiol the physiological stage seven out of 11 experiments,
and inhibin secretion increases, inhibiting further LH Table 2. The influence of feed intake on mean LH
and FSH release see Section 2.1, which probably plasma concentrations is less clear and mean LH is
induces atresia of the smaller follicles of the cohort. significantly reduced during feed restriction in only a
minority of experiments four out of 14 experiments, Table 2. Such a difference is probably due to
3. Main effects of nutrition on the methodological reasons as plasma LH between
