The Evolution of Genomic Imprinting – A Marsupial Perspective

Abstract

Genomic imprinting is a medically significant epigenetic trait in which genes are expressed from only one of the two alleles, according to their parent of origin. Among vertebrates, imprinted gene expression has been found only in the live-bearing therian mammals – eutherians (placental mammals) and marsupials. Because marsupials are so distantly related to eutherians, comparisons of imprinting between the two mammalian infraclasses are particularly valuable. However, the popular mammalian model organisms (humans, mice and domestic mammals) are all eutherian, so imprinting in marsupials has not received the attention it deserves. Research gathered over some years shows that marsupial orthologues of many imprinted domains in eutherians, such as the well characterised IGF2/H19 and PEG10 domains, comprise fewer imprinted genes. Other eutherian imprinted domains, such as the X-inactivation centre, Callipyge and Prader-Willi/Angleman syndrome domains, are either completely absent in marsupials or are not imprinted. The occurrence of imprinting in marsupials (with some imprinted genes) and eutherians (with many imprinted genes) contrasts with the likely absence of imprinting in egg-laying vertebrates (monotreme mammals, birds and reptiles). The acquisition of imprinting by therian mammals correlates with increased dependence on placentation for early development and coincides with the acquisition of a unique repeat content within the genome and germline expression of BORIS. Analysis of the evolutionary trajectory of these traits offers us insights into how and why genomic imprinting evolved in mammals.