REIkiz%imN

SCIENCE
ELSEVIER Animal ReproductionScience 42 (1996) 25-34

Nutrition and reproduction

J.J. Robinson
Scottish Agricultural College. Ferguson Building, Craibstone Estate, Bucksburn, Aberdeen AB.21 9YA, UK

Abstract

Through their influence on embryonic and early fetal development dietary nutrients affect the
size, vigour and viability of the newborn and, in the case of sheep, adult ovulation rates.
Nutritional regimens that impair post-natal growth reduce ovarian follicular development and
delay puberty but have little, if any, effect on either N-methyl-D-aspartate stimulated GnRH
release or the pituitary content of gonadotrophins. Nutritional effects on ovulation rate in ewes are
not always accompanied by shifts in circulating FSH concentrations. Instead they may operate
through altered ovarian hormone feedback mechanisms that influence the duration of exposure of
the gonadotrophin-dependent follicles to FSH or through threshold-reducing actions of specific
nutrients and dietary-induced metabolites on the amount of FSH needed to support the go-
nadotrophin-dependent follicles. Recent results suggest that the enhanced faecal excretion of
oestradiol by well-fed ewes may increase ovulation rate by reducing ovarian oestradiol feedback.
In the post-partum period, the key hypothalamic and pituitary secretions for successful
ovulation develop normally despite undernutrition but ovulation is prevented by failure of GnRH
release with, in the case of suckler beef cows, a delay in oestrus arising from the repeated
development and atmsia of dominant ovarian follicles. This effect is accentuated in cows that are
in poor body condition at calving. Alleviating the energy deficits of high-yielding dairy cows in
early lactation by giving supplements of dietary fat can reduce the interval to first oestrus but
subsequent fertility can be impaired. Loss of body protein delays oestrous cyclicity; paradoxically
attempts to correct this loss in ruminants by feeding diets high in rumen undegradable protein can
stimulate body fat mobilization and milk production with detrimental effects on rebreeding.
Excess rumen degradable protein and high feeding levels reduce embryo survival, the latter by
suppressing chculating progesterone concentrations. In superovulated ewes diet-induced reduc-
tions in progesterone concentrations during oocyte maturation can impart a legacy of developmen-
tal retardation leading to decreased embryo survival. In late pregnancy, undernutrition decreases
uterine blood flow, fetal insulin and IGF-I concentrations and impairs growth and development. In
the newborn, low insulin and a low selenium and iodine status inhibit thermogenesis from brown
adipose tissue. Insulin may also be important in conveying information on nutritional status to the
GnRH neurones thereby initiating the cascade of events that is required for successful mproduc-
tion in both sexes.

Keywords: Nubition; Ovulation; Embryo; Fetus; Neonate; Puberty

0378-4320/%/$15.00 0 1996Elsevier Science B.V. All rights nxerved.

PII SO378-4320(96)01526-6
26 J.J. Robinson/Animal Reproduction Science 42 (1996) 25-34

1. Introduction

Dietary nutrients promote the programming and expression of the metabolic pathways
that enable animals to achieve their genetic potential for reproduction. These pathways
are complex and in many cases they are not yet fully described. Thus the identification
of blood-borne metabolites that mediate, for example, the nutritional activation of the
GnRH pulse generator, is proving extremely difficult. On the other hand, important new
observations are being made on the effects of feeding level and specific dietary nutrients
during embryonic and early fetal life on subsequent reproductive performance. This
concept of early nutrition influencing later outcome is now becoming a major research
area (Lucas, 1992); so too is the quest to understand the molecular and cellular
mechanisms involved when alterations in the supply of nutrients evoke changes in
reproductive performance.

2. Early nutrition and later reproductive performance

In ewes, undernutrition during fetal and neonatal life reduces subsequent litter size
(reviewed by Robinson, 1990). Recent studies have demonstrated an effect of undemu-
trition (0.5 X maintenance) on the concentrations of oogonia in the ovine ovary as early
as Day 47 of fetal life (Borwick et al., 1994) and an associated postponement in the
arrest of ovarian meiotic activity on Day 62 (Borwick et al., 1995).
An important component of reproduction is viability at birth. There is evidence in
ewes that sub-clinical cobalt deficiency during early pregnancy, although having no
effect on lamb birthweights, is associated with reduced lamb vigour at birth and a
depression in passive immunity to disease (Fisher and MacPherson, 1991). While the
mechanisms involved have not been identified, this is another example of the early
nutritional programming of a later response; correction of the cobalt deficiency later on
in pregnancy did not improve’vigour at birth.
In vitro embryo culture systems are providing new examples of early programming
effects that are likely to be nutritional in origin. Following a period of in vitro culture,
early cleavage-stage sheep embryos produce oversize lambs (5.6 vs. 4.8 kg; heaviest
lamb 11,O kg) with a higher incidence of dystocia-related neonatal mortality (20 vs.
3.4%) than those from in vivo derived control embryos (Walker et al., 1992). More
recently, Thompson et al. (1994) found that the birthweights of lambs from embryos
cultured in synthetic oviduct fluid @OF) medium supplemented with human serum (HS)
were greater than those from spontaneously-ovulating ewes (4.2 f 0.2 vs. 3.4 rt 0.2 kg)
or those derived from embryos cultured in SOF supplemented with amino acids and
bovine serum albumin (3.5 f 0.2 kg). Although the causal factor in the human serum
has not been identified, McEvoy et al. (1995a) noted that the addition of HS to SOF
medium resulted in the production of high concentrations of ammonia (- 140 pmol
1-i) in the culture medium and, in an in vivo study, Bishonga et al. (1994) found that
while elevated plasma ammonia concentrations (100-150 pmol 1-l) induced a high
incidence of embryo mortality, they also appeared to be associated with fetal oversize in
 J.J. Robinson/Animal Reproduction Science 42 (1996) 25-34 27

those that survived. The phenomenon of fetal oversize may not be restricted therefore to
in vitro embryo culture but may also arise from in vivo nutritional influences.

3. Nutritional effects on puberty

Apart from the studies of Foster et al. (1988) demonstrating that parenteral infusion
of a dextrose-amino acid mixture was as effective as high-plane feeding in sustaining a
high LH pulse frequency in ewe lambs and those of Phillippo et al. (1987) suggesting
that a molybdenum-induced interference in LH secretion delayed puberty in heifers,
investigations into the effects of nutrition on the attainment of puberty are confined
largely to those involving feeding-level induced alterations in growth rate. At the
ovarian level, low feed intakes that delay puberty are accompanied by reduced follicular
development which, in the case of heifers, is associated with smaller dominant follicles
(Bergfeld et al., 1994). This occurs despite the availability of adequate pituitary
gonadotrophins, as judged by the response of the pituitary gland to a physiological dose
of GnRH, although realimentation does result in further increases in the levels of LH (Y,
LH /3 and FSHP mRNA (Landefeld et al., 1989). It also occurs in the presence of
adequate G&H, based on its release by N-methyl-D-aspartate, an agonist of the
stimulatory neurotransmitter, glutamate (Ebling et al., 1990).
The neurotransmitters involved in the nutritional activation of the GnRH pulse
generator in pubertal animals are still the subject of speculation and their action may
involve a balance between inhibitors and stimulators (reviewed by Adam and Robinsan,
1994). Although nutritional studies of ewe lambs and gilts appear to rule out the opioids,
their interaction with neuropeptide Y (NPY) may be relevant. McShane et al. (1993)
reported levels of mRNA for proopiomelanocortin (POMC), the precursor of the opioid
peptide, P-endorphin, that were - 50% lower in the hypothalami of feed-restricted
compared with well-fed lambs, leading them to suggest that the inhibitory effects of
NPY neurons on GnRH release may be enhanced by the decrease in P-endorphin.
Blood-borne metabolites that reflect nutritional status and are involved in the control
of GnRH release are also subjects of speculation. The observations of Hall et al. (1992)
demonstrating a stimulatory effect of abomasal infusion of tyrosine on LH pulse
frequency in growth-restricted ewe lambs imply that this amino acid may function as a
nutritional signal influencing the central nervous control of GnRH release. Other
blood-borne metabolites that have been considered are insulin and the insulin-like
growth factors (IGFs) but again their role, if any, is unclear in that neither parenteral
(Suttie et al., 1991) nor intra-cerebroventricular (Hileman et al., 1993) infusion altered
LH secretion in growth-restricted female lambs.

4. Nutrition and ovulation rate

Scaramuzzi et al. (1993) suggested that alterations in ovulation rate in general occur
when the duration of the ‘window’ of time in which gonadotrophin-dependent follicles
are viable is increased or when there is an increase in the rate of follicular through-put
28 J.J. Robinson/Animal Reproduction Science 42 (19%) 25-34

without any shift in the duration of the ‘window’. In the case of ovulatory responses to
nutrition, elements of both mechanisms could operate. Via its effects on the ovarian
hormone feedback control of gonadotrophin secretion, nutrition may, on the one hand,
alter the level and duration of exposure of gonadotrophin-dependent follicles to FSH. On
the other hand since the effects of nutrition on circulating FSH concentrations remains
equivocal it also has been suggested that nutrients (glucose, amino acids) and nutrient-
related metabolites (insulin, growth hormone, the IGFs and now their binding proteins)
that have been implicated in the ovulatory response to nutrition, may operate at the level
of the ovary to decrease the amount of FSH needed to support the gonadotrophin-depen-
dent follicles (Downing and Scaramuzzi, 1991). With regard to the ovarian hormone
feedback mechanism, oestradiol-17p may play an important role in mediating so-called
‘nutritional effects’ in that its enhanced faecal excretion in well-fed ewes leads to
reduced circulating plasma concentrations (Adams et al., 1994) and an associated
reduction in oestradiol feedback that would be expected to enhance ovulation rate
(Payne et al., 1991).
In an attempt to identify blood-borne metabolites that mediate the stimulatory effect
of a lupin-grain supplement on mean ovulation rate (2.5 vs. 1.9) in ewes, Downing et al.
(1995a) suggested direct ovarian action through increased glucose availability. The
accompanying sustained increase in plasma insulin also was observed when ovulation
rate was increased by either intravenous infusion of glucose (Downing et al., 1995b) or
the branched chain amino acids, leucine, isoleucine and valine (Downing et al., 1995c)
for 5 days in the late luteal phase of the oestrous cycle. Using the auto-transplanted
ovary model, Downing (1994) demonstrated that while infusions of glucose or insulin
alone had no effect on ovarian steroid secretion, their combined infusion decreased the
secretion of both androstenedione and oestradiol in response to a G&I-I-stimulated LH
pulse, again implying the involvement of altered steroid feedback in the ovulatory
response. In a practical attempt to boost glucose supply, Landau et al. (1995) found that
the daily provision of 100 g of rumen undegradable starch increased mean ovulation rate
(3.29 vs. 2.46) in carriers of the FecB gene but not in non-carriers (1.44 vs. 1.361,
suggesting that an important feature of responses in ovulation rate to nutrient supply
may be the ovulation potential of individual animals.

5. Nutrition and the parturition to rebreediig interval

The rapid fall in oestradiol concentrations at parturition removes its negative feed-
back on the hypothalamic-pituitary axis, thus stimulating the synthesis of mRNAs for
the gonadotrophins. This is followed by a rise in pituitary LH/FSH, an increase in the
activity of the GnRH pulse generator, development of ovarian follicles and, in the case
of the cow, selection of a dominant follicle for ovulation. Although many of these events
can take place during periods of undernutrition the final one, ovulation, is precluded by
inadequate GnRH secretion. Thus in post par-turn suckler beef cows, Stagg et al. (1995)
found that the mean interval from calving to first ovulation was 25 days longer for those
receiving 80 as opposed to 120 MJ of ME daily, but the timing of the development of
 JJ. Robinson/Animal Reproduction Science 42 (19%) 25-34 29

dominant follicles and their growth characteristics were not significantly affected by
nutrition; rather the extended period of anoestrus caused by undernutrition was due to
repeated development and atresia of dominant follicles.
There is now a considerable amount of data demonstrating an interaction between
body condition at calving and subsequent feeding level in terms of their influence on the
interval to first post-partum oestrus. By way of example, Wright et al. (1992) found that
thin cows (condition score 2.2) on a low compared with a high intake of ME (60 vs. 115
MJ daily) had a longer interval (116 vs. 89 days) whereas in fat cows (condition score
2.9) the difference between the low and high feeding levels in the duration of
post-partum anoestrus was small (89 vs. 80 days) and not significant.
In high-yielding dairy cows, the magnitude of the energy deficit during the first 2 to 3
weeks after calving is closely correlated with the interval to first oestrus. On the
assumption that body lipid is the sole component of the energy deficit in early lactation,
supplements of dietary fat that are protected from hydrolysis in the rumen have been
tested for their efficacy in reducing the calving to rebreeding interval. The results of
these studies have been equivocal (Robinson, 1990; Lucy et al., 1992a) with, in some
circumstances, the advantages in the initiation of normal oestrous cyclicity outweighed
by poorer fertility, possibly arising from a reduction in embryo survival due to excessive
oestrogen production by the increased number of large follicles ( > 15 mm diameter) in
cows receiving dietary supplements of fat (Lucy et al., 1991).
Low protein intakes can reduce the incidence of behavioural oestrus and conception
in beef cows but due to the stimulatory effect of digestible undegradable protein (DUP)
on milk production and therefore on the magnitude of the deficit in energy balance, high
DUP diets can also have a detrimental effect. This is exemplified by the significant
increase in the interval to first oestrus when a high as opposed to a low DUP diet was
fed to suckler cows that were in low body condition at mating (Sinclair et al., 1994).
Aside from this indirect adverse effect of high DUP on the resumption of oestrous
cyclicity in cattle, a direct effect of dietary protein on the protein status of the animal is
likely to be a major determinant of the impact of dietary protein on the post-partum
resumption of oestrous cyclicity. The significant relationship, I = 3.44 PL+ 9.6(King,
1987), between the weaning to oestrous interval (I days) and the estimated loss of body
protein in primiparous sows during lactation (PL kg) as a result of feeding low protein
diets, confirms this assertion.
Theories about the mechanisms involved in monitoring, processing and transmitting
information on nutritional status to the GnRH neuron during the post-partum period
remain speculative. In the absence of detectable effects on LH secretion, undernutrition
slows follicular growth in post-partum dairy cows. This shift in follicular dynamics is
accompanied by reduced IGF-1 concentrations in plasma and a reduced oestrogen to
progesterone ratio in the follicular fluid of dominant follicles (Lucy et al., 1992b). Thus
the nutritional modulation of follicular development involves both intra- and extra-ovarian
growth factors with the probability that IGF-I is only one of many; other likely
candidates are the IGF binding proteins (Echternkamp et al., 1994), transforming growth
factor a , epidermal growth factor and other members of the transforming growth factor
p family, for which knowledge of the effects on follicular development is still largely
confined to in vitro studies (see Webb et al., 1994).
30 J.J. Robinson/Animal Reproduction Science 42 (1996) 25-34

6. Nutrition and embryo survival

The effects of nutrition on embryo survival were reviewed by Robinson (1990) and
more recently by Ashworth (1994). Briefly, extremes in the level of feeding are
detrimental to embryo survival, so too are extremes in the supply of specific dietary
nutrients such as vitamins, trace elements and protein. For many of the vitamins and
trace elements the effects of a deficiency are understandable in view of their roles in
metabolism. The retinoids are the main metabolites of vitamin A and are involved in cell
proliferation and differentiation, the expression of growth factors, gene transcription and
steroidogenesis, all of which play important roles in embryo survival. Folic acid, for
which there is evidence of improved prenatal survival, is essential for nucleic acid
synthesis, and vitamin C appears to enhance luteal function, perhaps through its cofactor
role in steroidogenesis which again would explain its reputed beneficial effect in
maintaining early pregnancy in cattle. Correction of selenium deficiency in ewes reduces
embryo mortality during implantation. It also increases fertilization rate, probably via its
stimulating effect on uterine contractions and sperm transport, an effect which may be
particularly important in combating the adverse influences on sperm transport and
fertilization rate of the hostile uterine environment that occurs when animals are
superovulated.
Recently, attempts have been made to identify the mechanisms involved in the
adverse effects of high protein diets on the fertility of dairy cows. Elrod and Butler
(1993) found that high intakes of rumen degradable protein (RDP), leading to excess
rumen ammonia production, were associated with a reduction in the pH of the uterine
environment, and Elrod (1992) reported that ammonia and urea differentially affected
endometrial ion transport. For high RDP diets which result in excessive ammonia
production in the rumen, its hepatic detoxification is likely to impose an additional
demand for amino acids (Lobley et al., 1995). This implies that the provision of
supplementary amino acids in the form of dietary proteins of low ntmen degradable
status may avoid the adverse effects of excess RDP on the uterine environment and
embryo survival.
The mechanisms involved in the reduction of embryo survival by high-plane feeding
in early pregnancy are also the subject of speculation. The stimulatory effects of
high-plane feeding on the metabolic clearance rate of progesterone (Parr et al., 1993,
ewe; Prime and Symonds, 1993, gilt) and the concomitant reduction in progesterone
concentrations at the time (Days 11 and 12 post mating in the ewe> when the embryo is
extremely sensitive to low concentrations (s 2 ng ml- ’ in the peripheral circulation)
undoubtedly are involved (Parr, 1992). However the primary sites of action of proges-
terone differ between species (Heap et al., 1992), thus making it difficult to identify its
role in promoting the numerous paracrine pathways that link endometrial function with
embryo survival.
Dietary-induced suppression of circulating progesterone during oocyte maturation in
superovulated ewes primed with a single CIDR device (0.3 g progesterone) can impart a
legacy of developmental retardation which leads to decreased embryo survival (McEvo~
et al., 1995b). Again the causal mechanisms are the subject of speculation (McEvo~ et
al., 1995b), but may involve abnormal oestradiol:progesterone ratios which could disrupt
 JJ. Robinson/Animal Reproduction Science 42 (1996) 25-34 31

oocyte maturation by way of incomplete or late closure of gap junctions within the
follicle. Alternatively, the expression of maternal mRNAs required for matemally-regu-
lated development up to mid-blastocyst stage may be impaired by low progesterone. In
view of the detrimental effects of the diet-induced suppression of preovulatory proges-
terone on embryonic cell number and protein synthesis in the experiments of McEvoy et
al. (1995b), some of the developmental retardation and reduced embryo survival may be
due to either inadequate stimulation of ‘early’ response genes such as c-myc, which is
progesterone-dependent, or abnormal endometrial expression of erb-A, another ‘early’
response gene, which may modify the function of the progesterone receptor (Heap et al.,
1992).

7. Nutritional effects on fetal and neonatal metabolism

Undernutrition decreases uterine blood flow and the accompanying decrease in fetal
insulin and IGF-1 coupled with increases in growth hormone, adrenocorticotrophin and
corticosterone impair fetal growth and development. Fetal urea concentrations increase
during periods of undernutrition, reflecting increased gluconeogenesis by the fetus from
amino acids (Bell, 1993). This observation provides an explanation for the beneficial
effect of UDP supplements in maintaining lamb birthweights in ewes receiving sub-opti-
mal levels of energy during late pregnancy.
In newborn lambs, low insulin, high corticosterone and a low selenium and/or iodine
status inhibit thermogenesis from brown adipose tissue, BAT (Robinson, 1990; Symonds,
1995; Robinson and Symonds, 1995). The vital role that selenium plays in the
thermogenic response of BAT was demonstrated by the finding that the iodothyronine
5deiodinase enzyme which converts T4 to the active T3 in extra-thyroidal tissues
including BAT, is selenium-dependent (Arthur, 1991). Thus lambs from ewes fed diets
containing either inadequate levels of selenium (Donald et al., 1994) or high concentra-
tions of naturally occurring selenium antagonists such as the cyanogenetic glycosides
(Gutzwiller, 1993) have high T4, low T3 concentrations and a reduced viability at birth.

8. Nutritional effects on male reproduction

The inter-relationships between nutrition, growth rate and age at puberty in the male
are similar to those in the female. Briefly, males reared on low as opposed to high
planes of nutrition reach puberty at older ages and lighter body-weights and in seasonal
breeders such as sheep, goats and deer, undernutrition can delay puberty for a complete
year. In mature rams, there is a 6 to 7 week delay in the response in spermatozoa
numbers to diet, reflecting the time it takes for the development of spherical spermatids
in the germinal epithelium to fully mature spermatozoa in the distal cauda epididymidis.
Evidence for direct effects of nutrition on testis growth and production of spermatozoa
in the absence of alterations in the G&H-gonadotrophin system, led Martin and
Walkden-Brown (1995) to develop the concept that both GnRH independent and
dependent pathways are involved in nutritional effects on spermatogenesis. Identification
32 JJ. Robinson/Animal Reproduction Science 42 (19%) 25-34

of the blood-borne metabolites that mediate the two pathways is still by way of
association rather than causal. If IGF-1 is involved in the GnRH-independent pathway, it
would appear to be at the intratesticular level (Martin and Walkden-Brown, 1995). For
the G&I-I-dependent pathway the stimulatory effect of intracerebral infusions of insulin
on LH secretion in mature rams (Miller et al., 1995) implies a role for insulin in
conveying information on nutritional status to the GnRH neurones.

Acknowledgements

The Scottish Agricultural College receives financial support from the Scottish Office
Agriculture, Environment and Fisheries Department.

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