The origin and evolution of genomic imprinting and viviparity in mammals

Abstract

Genomic imprinting is widespread in eutherian mammals. Marsupial mammals also have genomic imprinting, but in fewer loci. It has long been thought that genomic imprinting is somehow related to placentation and/or viviparity in mammals, although neither is restricted to mammals. Most imprinted genes are expressed in the placenta. There is no evidence for genomic imprinting in the egg-laying monotreme mammals, despite their short-lived placenta that transfers nutrients from mother to embryo. Post natal genomic imprinting also occurs, especially in the brain. However, little attention has been paid to the primary source of nutrition in the neonate in all mammals, the mammary gland. Differentially methylated regions (DMRs) play an important role as imprinting control centres in each imprinted region which usually comprises both paternally and maternally expressed genes (PEGs and MEGs). The DMR is established in the male or female germline (the gDMR). Comprehensive comparative genome studies demonstrated that two imprinted regions, PEG10 and IGF2-H19, are conserved in both marsupials and eutherians and that PEG10 and H19 DMRs emerged in the therian ancestor at least 160 Ma, indicating the ancestral origin of genomic imprinting during therian mammal evolution. Importantly, these regions are known to be deeply involved in placental and embryonic growth. It appears that most maternal gDMRs are always associated with imprinting in eutherian mammals, but emerged at differing times during mammalian evolution. Thus, genomic imprinting could evolve from a defence mechanism against transposable elements that depended on DNA methylation established in germ cells.

Epigenetics and developmental programming of welfare and production traits in farm animals

“…This observation confirmed an earlier report of abnormal hypomethylation of KvDMR1 and expression of KCNQ1OT1 in two of seven SCNT cloned calves and one of two IVP-derived calves (Hori et al 2010). Although generally highly conserved, there are also recognisable differences in imprinting within eutherian mammals that could account for many such differences between species, differential imprinting at the IGF2R locus being a case in point (Das et al 2009;Renfree et al 2013).…”

Using next-generation RNA sequencing to identify imprinted genes

“…In animals, genomic imprinting is only known in therian mammals, and most imprinted genes are expressed and imprinted in the brain and placenta (Pask, 2012;Keverne, 2013;Renfree et al, 2013). Having the full catalog of imprinted genes in several different mammalian species will greatly facilitate the understanding of many evolutionary questions about genomic imprinting, including but not limited to origin and fixation of genomic imprinting, conservation of degree of expression direction and imprinted genes, dynamic gain and loss of imprinting status on the mammalian phylogenetic tree and effect of loss of diploidy for imprinted genes in shaping the population genetic profile.…”

First principles of Hamiltonian medicine

“…Such effects are expected because during development, power over phenotypes is commonly (i) some function of time, because events earlier in ontogeny have larger, more-cascading effects, and (ii) some function of control over rates and patterns of cell and tissue proliferation, because this is how organisms grow and differentiate. This prediction is well supported by recent studies showing that in a wide range of human tissues, imprinted genes orchestrate stem cell replication versus inhibition [96][97][98], and by the observation that imprinted genes exert especially pervasive effects on placental development, at the start of fetal growth and development [99,100]. Imprintedgene conflicts will therefore be especially important in mediating causes of variation in physical health, because so many human health outcomes are highly dependent on early-life events and phenotypes such as placental function and birth weight [101], and on the roles of stem cells in tissue renewal and repair.…”