Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation.

Uterine crowding in the pig results in intrauterine growth restriction (IUGR), and permanently affects fetal muscle fibre development, representing production losses for the commercial pig herd. The present study sought to understand how different levels of uterine crowding in sows affects muscle fibre development in the early embryo at the time of muscle fibre differentiation and proliferation. Sows either underwent surgical, unilateral oviduct ligation (LIG; n = 10) to reduce the number of embryos in the uterus, or remained as intact, relatively-crowded controls (CTR; n = 10). Embryos and placentae were collected at Day 30 of gestation, and myogenic regulatory factor (MRF) transcript abundance was determined using real-time PCR for both myogenin (MYOG) and myoblast differentiation 1 (MYOD1). Unilateral tubal ligation resulted in lower numbers of embryos in utero, higher placental weights and a higher male : female sex ratio (P < 0.05). Relative MYOD1 expression was not different, but MYOG expression was higher (P < 0.05) in the LIG group embryos; predominantly due to effects on the male embryos. Relatively modest uterine crowding therefore affects MRF expression, even at very early stages of embryonic development, and could contribute to reported differences in fetal muscle fibre development, birthweight and thus post-natal growth performance in swine.

Macroenvironment effects on oocytes and embryos in swine.

As in other domestic mammals, the interaction between genotype and environment in swine has profound effects on the ultimate phenotype of the individual born. Interactions within the litter in utero add an additional level of complexity in a litter-bearing species like the pig. Nutritional manipulations during the preovulatory period affect the maturity of the follicle and enclosed oocyte, and the metabolic and endocrine mechanisms potentially mediating these effects have been described. Extensive research on lactational catabolism in the first parity sow has established an association between the development of immature follicles and oocytes, and the reduced fertility of these sows when bred at the first postweaning estrus. This negative impact of lactational catabolism appears to be exaggerated in contemporary dam-lines by a minimal delay between weaning and first estrus, further limiting the maturity of the follicle and oocyte at the time of ovulation. Metabolic programming may induce gender-specific loss of embryos by Day 30 and affects embryonic development directly, without significant effects on placental size. In contrast, inadvertent crowding of embryos in utero, particularly evident in a sub-population of mature sows with high ovulation rates and moderate to high embryonic survival to Day 30, significantly limits placental development of crowded litters. However, even at Day 30, moderate crowding in utero also appears to affect myogenesis in the embryo in a gender-specific manner. In the absence of compensatory placental growth after Day 30, classic measures of IUGR are evident in surviving fetuses at Day 90 and at term.

The biological basis for prenatal programming of postnatal performance in pigs.

The main purpose of this review is to discuss associations between within-litter variation in birth weight, and preweaning survival and postnatal growth in the pig, as the basis for suggesting that the developmental competence of pigs born, as well as the size of the litter, need critical consideration. Extremes of intrauterine growth retardation (IUGR) occur within a discrete subset of fetuses, substantially smaller than their littermates and commonly described as runt piglets. The lower preweaning growth of runt pigs cannot be entirely explained based on their lower birth weight, nor do they show full postnatal compensatory growth. Interestingly, this more complex reprogramming of development in runt pigs can already be identified by d 27 to 35 of gestation. Recently, we reported more universal IUGR effects in commercial dam-line sows, as an indirect response to selection for increased litter size. High ovulation rates (>30 ovulations) in a proportion of greater parity sows are associated with increased numbers of conceptuses surviving to d 30 of gestation, resulting in detrimental effects on placental development of uterine crowding in the early postimplantation period. In turn, this limits nutrient availability to the embryo during a critical period of myogenesis. Consequently, although a reduction in the number of conceptuses occurs by d 50, placental development in the surviving fetuses remains compromised, resulting in IUGR and reduced numbers of muscle fibers at d 90 and at birth, in all surviving littermates. These effects of uterine crowding on fetal and postnatal development are analogous to the detrimental effects of nutritional restriction in gestating sows on fetal myogenesis, birth weight, and postnatal growth. The incompatibility between increased numbers of conceptuses surviving to the postimplantation period, in the absence of increased uterine capacity, offers a biological explanation for increased variability in birth weight and postnatal growth performance reported in greater parity sows. We conclude that a strategy of introducing hyperprolific females into the breeding nucleus, as a means of increasing the numbers of pigs born, needs to be critically evaluated in the context of the overall efficiency of pork production.

Embryonic and fetal development in a commercial dam-line genotype.

During depopulation of a breeding unit within Swine Graphics Enterprises, extensive data were collected and used to examine relationships among ovulation rate, the pattern of prenatal loss, and placental and fetal development. Groups of Large White x Landrace females (n=447) were slaughtered between day 20-30, 50-55 or 85-90 of gestation, with approximately equal numbers of animals representing gilts and parity 1 (G/P1), parity 2-3 (P2/3), and parity >4 (P4+). Ovulation rate and embryo number were recorded for all animals. With the exception of the G/P1 animals, embryonic and placental weight were recorded for four conceptuses per sow on day 20-30; on day 85-90 two conceptuses per sow were dissected to determine placental and fetal development. Ovulation rate (22.7 +/- 0.2 overall) was higher (P <0.05) in P2/3 (23.6 +/- 0.4) and P4+ (24.7 +/- 0.4) than in G/P1 (20.2 +/- 0.5). Embryonic/fetal survival was 61.8 +/- 2.1% at day 20-30, 50.2 +/- 2.2% at day 50-55 and 48.7 +/- 1.9% at day 85-90 and the number of surviving conceptuses was higher (P <0.05) in the P2/3 sows than in other parity groups. There was no relationship between ovulation rate and number of live embryos at day 20-30 or 85-90. At day 20-30 and 85-90, embryo weight was positively correlated with placental weight, but neither placental weight nor embryonic/fetal weight was correlated with number of viable embryos. A parity by gestation day interaction existed; placental weight for P4+ (3.42 +/- 0.43 g) was less than for P2/3 (7.55 +/- 0.40 g) at day 20-30 (P <0.0001), whereas at day 85-90, placental weight of P2/3 (209.5 +/- 8.5 g) was less (P=0.05) than both G/P1 (235.7 +/- 7.3g) and P4+ (235.4 +/- 7.1 g). At day 85-90, fetal brain weight, relative to body weight (R2=0.61, P <0.0001), and fetal brain:liver weight ratio (R2=0.35; P <0.0001) were negatively related to mean fetal weight, and brain:liver weight ratio showed a trend towards a relationship with number of viable fetuses (P=0.08). Parity also affected brain:liver weight ratio (P=0.01). Clearly, high ovulation rates in the higher parity sows have the potential to cause excessive in utero crowding of conceptuses in the post-implantation period. Even with moderate crowding, increased brain:liver weight ratios in smaller fetuses in late gestation indicate that uterine capacity impacts fetal development as well as the number of surviving fetuses.

Number of conceptuses in utero affects porcine fetal muscle development.

Unmodified, third parity, control sows (CTR; n = 30) or sows subjected to unilateral oviduct ligation before breeding (LIG; n = 30), were slaughtered at either day 30 or day 90 of gestation and used to determine the effects of numbers of conceptuses in utero on prenatal, and particularly muscle fibre, development. Ovulation rate, number of conceptuses in utero, placental and fetal size, and (day 90 sows) fetal organ and semitendinosus muscle development were recorded. Tubal ligation reduced (P < 0.05) the number of viable embryos at day 30 and fetuses at day 90. Placental weight at day 30 and day 90, and fetal weight at day 90, were lower (P < 0.05) in CTR sows. All body organs except the brain were lighter, and the brain:liver weight ratio was higher in CTR fetuses (P < 0.05), indicative of brain sparing and intrauterine growth restriction in fetuses from CTR sows. Muscle weight, muscle cross-sectional area and the total number of secondary fibres were also lower (P < 0.05) in CTR fetuses. The number of primary fibres, the secondary:primary muscle fibre ratio, and the distribution of myosin heavy chain-Ibeta, -IIa, fetal and embryonic isoforms did not differ between groups. Thus, even the relatively modest uterine crowding occurring naturally in CTR sows negatively affected placental and fetal development and the number of secondary muscle fibres. Consequences of more extreme crowding in utero on fetal and postnatal development, resulting from changing patterns of early embryonic survival, merit further investigation.