Evolution of viviparity in mammals: What genomic imprinting tells us about mammalian placental evolution

Abstract

Genomic imprinting is an epigenetic mechanism of regulating parent-of-origin-specific monoallelic expression of imprinted genes in viviparous therian mammals such as eutherians and marsupials. In this review we discuss several issues concerning the relationship between mammalian viviparity and genomic imprinting, as well as the domestication of essential placental genes: why has the genomic imprinting mechanism been so widely conserved despite the evident developmental disadvantages originating from monoallelic expression? How have genomic imprinted regions been established in the course of mammalian evolution? What drove the evolution of mammalian viviparity and how have genomic imprinting and domesticated genes contributed to this process? In considering the regulatory mechanism of imprinted genes, reciprocal expression of paternally and maternally expressed genes (PEGs and MEGs respectively) and the presence of several essential imprinted genes for placental formation and maintenance, it is likely that complementary, thereby monoallelic, expression of PEGs and MEGs is an evolutionary trade-off for survival. The innovation in novel imprinted regions was associated with the emergence of imprinting control regions, suggesting that genomic imprinting arose as a genome defence mechanism against the insertion of exogenous DNA. Mammalian viviparity emerged in the period when the atmospheric oxygen concentration was the lowest (∼12%) during the last 550 million years (the Phanerozoic eon), implying this low oxygen concentration was a key factor in promoting mammalian viviparity as a response to a major evolutionary pressure. Because genomic imprinting and gene domestication from retrotransposons or retroviruses are effective measures of changing genomic function in therian mammals, they are likely to play critical roles in the emergence of viviparity for longer gestation periods.