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

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.