The coadaptation theory for genomic imprinting

Eleanor O'Brien, Jason Wolf

Research output: Contribution to journalArticle

Abstract

Imprinted genes are peculiar in that expression of the two copies differs depending on whether the copy was maternally or paternally inherited. The discovery of this striking pattern of gene expression inspired myriad evolutionary theories, the most successful of which identify scenarios that create an asymmetry between the maternally and paternally inherited gene copies that favors silencing of one of the copies. Most notably, imprinting can evolve when gene dosage affects kin interactions (typically involving conflict) or when silencing enhances coadaptation by coordinating traits expressed by interacting kin. Although we have a well-established theory for the former process (the “Kinship Theory”), the coadaptation process has only been explored for the specific case of interactions between mothers and offspring. Here, we fill this critical gap in our understanding by developing a general “Coadaptation Theory” that explains how imprinting can evolve to coordinate interactions between all types of relatives. Using a simple model in which fitness of an individual is determined by an interaction between its own phenotype (and hence genotype) and that of its social partner(s), we find that when the relatedness of interactants differs through their maternally versus paternally inherited gene copies, then selection favors expression of the allele through which relatedness is higher. The predictions of this Coadaptation Theory potentially apply whenever a gene underlies traits that mediate the outcome of conspecific interactions, regardless of their mechanism or the type of organism, and therefore provide a potential explanation for enigmatic patterns of imprinting, including those underlying adult traits. By providing simple testable predictions that often directly contrast with those derived from alternative theories, our model should play an important role in consolidating our understanding of the evolution of imprinting across genes and species, which will ultimately provide crucial insights into imprinted gene function and dysfunction.
Original languageEnglish
Pages (from-to)49-59
Number of pages11
JournalEvolution Letters
Volume1
Issue number1
DOIs
Publication statusPublished - 3 May 2017

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genomic imprinting
genes
gene dosage
prediction
kinship
alleles
phenotype
gene expression
genotype
organisms

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The coadaptation theory for genomic imprinting. / O'Brien, Eleanor; Wolf, Jason.

In: Evolution Letters, Vol. 1, No. 1, 03.05.2017, p. 49-59.

Research output: Contribution to journalArticle

O'Brien, Eleanor ; Wolf, Jason. / The coadaptation theory for genomic imprinting. In: Evolution Letters. 2017 ; Vol. 1, No. 1. pp. 49-59.
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