A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting

• Published in: PLoS biology Vol. 4; no. 12; p. e380
• Main Authors: Wolf, Jason B, Hager, Reinmar
• Format: Journal Article
• Language: English
• 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
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.0040380

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.