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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Published inPLoS biology Vol. 4; no. 12; p. e380
Main Authors Wolf, Jason B, Hager, Reinmar
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2006
Public Library of Science (PLoS)
Subjects
Adaptation, Biological
Animals
Biological Evolution
Development
Evolution
Female
Gene expression
Genetic Linkage
Genetics
Genetics/Genomics/Gene Therapy
Genomic imprinting
Genomic Imprinting - genetics
Genomics
Haplotypes
Humans
Hypotheses
Linkage Disequilibrium
Mammals
Maternal-Fetal Relations
Models, Genetic
Mothers
Offspring
Selection, Genetic
Theory
Biological Evolution
Genomic Imprinting
Animals
Maternal-Fetal Relations
Humans
Selection, Genetic
Adaptation, Biological
Female
Models, Genetic
Genetic Linkage
Linkage Disequilibrium
Online AccessGet full text
ISSN1545-7885
1544-9173
1545-7885
DOI10.1371/journal.pbio.0040380

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Abstract 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.
AbstractList 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.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.
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.
  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.
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. This theoretical paper demonstrates that maternal-offspring coadaptation (the selection for gene combinations of parents and offspring) could select for genomic imprinting of the offspring trait.
Audience Academic
Author Hager, Reinmar
Wolf, Jason B
AuthorAffiliation University of Edinburgh, United Kingdom
Faculty of Life Sciences, The University of Manchester, Manchester, United Kingdom
AuthorAffiliation_xml – name: Faculty of Life Sciences, The University of Manchester, Manchester, United Kingdom
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  surname: Wolf
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/17105351$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2006 Public Library of Science
2006 Wolf and Hager. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Wolf JB, Hager R (2006) A Maternal-Offspring Coadaptation Theory for the Evolution of Genomic Imprinting. PLoS Biol 4(12): e380. doi:10.1371/journal.pbio.0040380
2006 Wolf and Hager. 2006
Copyright_xml – notice: COPYRIGHT 2006 Public Library of Science
– notice: 2006 Wolf and Hager. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Wolf JB, Hager R (2006) A Maternal-Offspring Coadaptation Theory for the Evolution of Genomic Imprinting. PLoS Biol 4(12): e380. doi:10.1371/journal.pbio.0040380
– notice: 2006 Wolf and Hager. 2006
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DocumentTitleAlternate Maternal-Offspring Coadaptation Favors Imprinting
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Issue 12
Keywords Biological Evolution
Genomic Imprinting
Animals
Maternal-Fetal Relations
Humans
Selection, Genetic
Adaptation, Biological
Female
Models, Genetic
Genetic Linkage
Linkage Disequilibrium
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
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Snippet Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological...
  Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological...
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StartPage e380
SubjectTerms Adaptation, Biological
Animals
Biological Evolution
Development
Evolution
Female
Gene expression
Genetic Linkage
Genetics
Genetics/Genomics/Gene Therapy
Genomic imprinting
Genomic Imprinting - genetics
Genomics
Haplotypes
Humans
Hypotheses
Linkage Disequilibrium
Mammals
Maternal-Fetal Relations
Models, Genetic
Mothers
Offspring
Selection, Genetic
Theory
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Title A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting
URI https://www.ncbi.nlm.nih.gov/pubmed/17105351
https://www.proquest.com/docview/1292131286
https://www.proquest.com/docview/68294625
https://pubmed.ncbi.nlm.nih.gov/PMC1635750
https://doaj.org/article/1de884eb401648f2b9e0ed2454bf1854
http://dx.doi.org/10.1371/journal.pbio.0040380
Volume 4
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