A maternal-offspring coadaptation theory for the evolution of genomic imprinting.

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother-offspring interactions. There are several competing theories attempting to explain the evolution...

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Main Authors: Jason B Wolf, Reinmar Hager
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2006-11-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC1635750?pdf=render
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author Jason B Wolf
Reinmar Hager
author_facet Jason B Wolf
Reinmar Hager
author_sort Jason B Wolf
collection DOAJ
description Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother-offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.
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spelling doaj.art-1de884eb401648f2b9e0ed2454bf18542022-12-21T18:23:03ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852006-11-01412e38010.1371/journal.pbio.0040380A maternal-offspring coadaptation theory for the evolution of genomic imprinting.Jason B WolfReinmar HagerImprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother-offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.http://europepmc.org/articles/PMC1635750?pdf=render
spellingShingle Jason B Wolf
Reinmar Hager
A maternal-offspring coadaptation theory for the evolution of genomic imprinting.
PLoS Biology
title A maternal-offspring coadaptation theory for the evolution of genomic imprinting.
title_full A maternal-offspring coadaptation theory for the evolution of genomic imprinting.
title_fullStr A maternal-offspring coadaptation theory for the evolution of genomic imprinting.
title_full_unstemmed A maternal-offspring coadaptation theory for the evolution of genomic imprinting.
title_short A maternal-offspring coadaptation theory for the evolution of genomic imprinting.
title_sort maternal offspring coadaptation theory for the evolution of genomic imprinting
url http://europepmc.org/articles/PMC1635750?pdf=render
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