Review: Maternal programming of development in the pig and the lactocrine hypothesis

Abstract

Maternal effects on development are profound. Together, genetic and epigenetic maternal effects define the developmental trajectory of progeny and, ultimately, offspring phenotype. Maternally provisioned environmental conditions and signals affect conceptus, fetoplacental and postnatal development from the time of conception until weaning. In the pig, reproductive tract development is completed postnatally. Porcine uterine growth and uterine endometrial development occur in an ovary-independent manner between birth (postnatal day = PND 0) and PND 60. Milk-borne bioactive factors (MbFs), exemplified by relaxin, communicated from lactating dam to nursing offspring via a lactocrine mechanism, represent an important source of extraovarian uterotrophic support in the neonatal pig. Lactocrine deficiency from birth affects both the neonatal porcine uterine developmental program and trajectory of uterine development, with lasting consequences for endometrial function and uterine capacity in adult female pigs. The potential lactocrine signaling window extends from birth until the time of weaning. However, it is likely that the maternal lactocrine programming window – that period when MbFs communicated to nursing offspring have the greatest potential to affect critical organizational events in the neonate – encompasses a comparatively short period of time within 48 h of birth. Lactocrine deficiency from birth was associated with altered patterns of endometrial gene expression in neonatally lactocrine-deficient adult gilts during a critical period for conceptus–endometrial interaction on pregnancy day 13, and with reduced litter size, estimated at 1.4 pigs per litter, with no effect of parity. Data were interpreted to indicate that reproductive performance of female pigs that do not receive sufficient colostrum from birth is permanently impaired. Observations to date suggest that lactocrine-dependent maternal effects program postnatal development of the porcine uterus, endometrial functionality and uterine capacity. In this context, reproductive management strategies and husbandry guidelines should be refined to ensure that such practices promote environmental conditions that will optimize uterine capacity and fecundity. This will entail careful consideration of factors affecting lactation, the quality and abundance of colostrum/milk, and practices that will afford neonatal pigs with the opportunity to nurse and consume adequate amounts of colostrum.

Effects of colostrum instead of formula feeding for the first 2 days postnatum on whole-body energy metabolism and its endocrine control in neonatal calves

“…The effect of colostral adiponectin on metabolic development in neonatal calves is not yet clear, but adiponectin may influence neonatal energy metabolism by affecting insulin action (Havel, 2002;Yamauchi and Kadowaki, 2013). In addition, lactocrine maternal programming of neonatal reproductive tract development has been discussed in piglets (Bagnell and Bartol, 2019).…”

Post-natal Growth Retardation Associated With Impaired Gut Hormone Profiles, Immune and Antioxidant Function in Pigs

“…The intrauterine growth restriction (IUGR) pigs also exhibit lower diversity and different taxonomic abundances of gut microbiota (3). Although possible causes of PGR have been discussed, such as placental insufficiency (4), pathogen burden (5), gut mucosal barrier dysfunction (6), parental genetic disruption (7), and abnormal maternal lactocrine programming (8), the question remains largely unsolved as to the assessment of the common markers between PGR pigs and pigs with normal growth. It is important to seek the possible intervening targets to enhance growth in poorly performing piglets, ensuring a good growth rate post-weaning (9, 10).…”

Bioactive compounds in mothers milk affecting offspring outcomes: A narrative review

“…2 Offspring organ development spans the prenatal through the postnatal period including key developmental and maturation events occurring in the first days to months after birth ranging from completion of adipocyte development in the first months to ongoing islet and hepatic development until beyond ~2 years of life, after weaning has occurred. 2,9 Regulation of energy homeostasis, metabolism and appetite is governed by the ongoing development of the hypothalamus, liver, muscle, pancreas, gut and adipose tissue that continues during the postnatal stage, but with timing that varies between altricial (incapable of movement after hatching, needing extensive parental care) and precocial (capable of movement upon hatching) species. 10 While organ development and differentiation are well-organized, controlled and regulated processes, disruptions or alterations in signalling events precipitated by milk factors can impact downstream development.…”