Post-natal imprinting: evidence from marsupials

Abstract

Genomic imprinting has been identified in therian (eutherian and marsupial) mammals but not in prototherian (monotreme) mammals. Imprinting has an important role in optimising pre-natal nutrition and growth, and most imprinted genes are expressed and imprinted in the placenta and developing fetus. In marsupials, however, the placental attachment is short-lived, and most growth and development occurs post-natally, supported by a changing milk composition tailor-made for each stage of development. Therefore there is a much greater demand on marsupial females during post-natal lactation than during pre-natal placentation, so there may be greater selection for genomic imprinting in the mammary gland than in the short-lived placenta. Recent studies in the tammar wallaby confirm the presence of genomic imprinting in nutrient-regulatory genes in the adult mammary gland. This suggests that imprinting may influence infant post-natal growth via the mammary gland as it does pre-natally via the placenta. Similarly, an increasing number of imprinted genes have been implicated in regulating feeding and nurturing behaviour in both the adult and the developing neonate/offspring in mice. Together these studies provide evidence that genomic imprinting is critical for regulating growth and subsequently the survival of offspring not only pre-natally but also post-natally.

The evolution of genomic imprinting: Epigenetic control of mammary gland development and postnatal resource control

“…We support the idea first proposed for marsupial mammals (Stringer et al, ), that the mammary gland represents the functional equivalent of the placenta in the postnatal stage of eutherian mammals. Both these organs support the normal growth and development of the offspring.…”

“…In marsupials, a smaller subset of genes is imprinted compared to eutherian mammals, pregnancy is shorter, and the major provision of nutrition is supplied through suckling, with the mammary gland delivering milk to the altricial neonate. Renfree and coauthors identified the specific imprinting of insulin ( Ins2 in mice) and IGF2 in this tissue (Stringer et al, ), and proposed that the marsupial mammary gland would therefore be a preferred site of imprinting because of its predominant role in nutritional support of its altricial neonate (Stringer et al, ). They have proposed that imprinting in the marsupial mammary gland parallels eutherian placenta imprinting.…”

“…However, similar to the placenta supporting growth and development of the offspring prenatally, the mammary gland nourishes the offspring postnatally, practically extending maternal provisioning to the neonate. From a functional perspective, we hypothesize that any organ that regulates growth via mother–offspring nutrient exchange would depend heavily on genomic imprinting, as has been proposed from marsupial studies where most nutrient transfer between mother and fetus occurs ex utero (Stringer, Pask, Shaw, & Renfree, ). Most studies on genomic imprinting have focused on prenatal development, but postnatal development is also critical in influencing adult health status (Martin‐Gronert & Ozanne, ).…”

The coadaptation theory for genomic imprinting

“…Both the Kinship and Maternal‐Offspring Coadaptation Theories were challenged by the discovery that many genes show imprinted expression after individuals are no longer receiving parental care (Wilkinson et al ), including many expressed in the brain that affect social behavior (Davies et al ; Wilkinson et al ; Garfield et al ), and several expressed in the mammary gland (Stringer et al , ; Cowley et al ). The Kinship Theory has been generalized to include all interactions between relatives, with selection for imprinting resulting from relatedness asymmetries (such as those arising from sex‐biased dispersal or reproductive success) that generate conflict over the expression level favored by the matrigenic and patrigenic gene copies (Úbeda and Gardner , ).…”

Genomic imprinting: theories and data

“…The paper by Stringer et al (2014) notes that imprinting has a critical role in eutherian pregnancy, with most imprinted genes expressed in the placenta and fetus. In marsupials, however, pregnancy is much shorter and the part of the eutherian placenta in supplying nutrition to the developing fetus is instead played by the mammary gland delivering milk to the altricial neonate.…”