Abstract

Epigenetic regulation in mammals begins in the first stages of embryogenesis. This prenatal programming determines, in part, phenotype expression in adult life. Some species, particularly dairy cattle, are conceived during the maternal lactation, which is a period of large energy and nutrient needs. Under these circumstances, embryo and fetal development compete for nutrients with the mammary gland, which may affect prenatal programming and predetermine phenotype at adulthood. Data from a specialized dairy breed were used to determine the transgenerational effect when embryo development coincides with maternal lactation. Longitudinal phenotypic data for milk yield (kg), ratio of fat-protein content in milk during first lactation, and lifespan (d) from 40,065 cows were adjusted for environmental and genetic effects using a Bayesian framework. Then, the effect of different maternal circumstances was determined on the residuals. The maternal-related circumstances were 1) presence of lactation, 2) maternal milk yield level, and 3) occurrence of mastitis during embryogenesis. Females born to mothers that were lactating while pregnant produced 52 kg (MonteCarlo standard error; MCs.e. = 0.009) less milk, lived 16 d (MCs.e. = 0.002) shorter and were metabolically less efficient (+0.42% milk fat/protein ratio; MCs.e.<0.001) than females whose fetal life developed in the absence of maternal lactation. The greater the maternal milk yield during embryogenesis, the larger the negative effects of prenatal programming, precluding the offspring born to the most productive cows to fully express their potential additive genetic merit during their adult life. Our data provide substantial evidence of transgenerational effect when pregnancy and lactation coincide. Although this effect is relatively low, it should not be ignored when formulating rations for lactating and pregnant cows. Furthermore, breeding, replacement, and management strategies should also take into account whether the individuals were conceived during maternal lactation because, otherwise, their performance may deviate from what it could be expected.

Highlights

  • The first stages of mammalian fetal development are determinant for the adult offspring, as dramatic changes in DNA methylation occur which are responsible of cell differentiation of the embryo [1]

  • Lack of nutrients during pregnancy has been associated with an increased risk of suffering metabolic diseases in adult life

  • Phenotypic traits of milk yield (MY), fat/protein ratio in milk (FP) and functional lifespan (DIM) were previously adjusted by environmental and genetic effects: the additive genetic merit of the i-individual due to the action of the genes inherited from her parents via germ cells, and the environmental effects of age of the individual at first parity, combined effect of year-region at birth, and combined effect of herd-year of first parity

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Summary

Introduction

The first stages of mammalian fetal development are determinant for the adult offspring, as dramatic changes in DNA methylation occur which are responsible of cell differentiation of the embryo [1]. This methylation process begins with primordial germ cells having very low methylation levels, with gametogenesis parental imprinting tags are established, with substantially methylated but differing methylomes in the sperm and egg. In the pre-implantation early embryo, there is a wave of genome-wide demethylation that occurs rapidly in the paternal genome, except for centromeric, and comparative slowly in the maternal genome [2]. The maternal effects alter phenotypes in the offspring by changes in the epigenome during pregnancy and suckling [5,6]

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