Dataset Information

Evolutionary Quantitative Genetics of Genomic Imprinting.

ABSTRACT: Genomic imprinting shapes the genotype-phenotype relationship by creating an asymmetry between the influences of paternally and maternally inherited gene copies. Consequently, imprinting can impact heritable and nonheritable variation, resemblance of relatives, and evolutionary dynamics. Although previous analyses have identified some of the quantitative genetic consequences of imprinting, we lack a framework that cleanly separates the influence of imprinting from other components of variation, particularly dominance. Here we apply a simple orthogonal genetic model to evaluate the roles of genetic (additive and dominance) and epigenetic (imprinting) effects. Imprinting increases the resemblance of relatives who share the expressed allele, and therefore increases variance among families of full or half-siblings. However, only part of this increased variance is heritable and contributes to selection responses. When selection is within, or among, families sharing only a single parent (half-siblings), which is common in selective breeding programs, imprinting can alter overall responses. Selection is more efficient when it acts among families sharing the expressed parent, or within families sharing the parent with lower expression. Imprinting also affects responses to sex-specific selection. When selection is on the sex whose gene copy has lower expression, the response is diminished or delayed the next generation, although the long-term response is unaffected. Our findings have significant implications for understanding patterns of variation, interpretation of short-term selection responses, and the efficacy of selective breeding programs, demonstrating the importance of considering the independent influence of genomic imprinting in quantitative genetics.

SUBMITTER: O'Brien EK

PROVIDER: S-EPMC6325703 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Evolutionary Quantitative Genetics of Genomic Imprinting.

O'Brien Eleanor K EK Wolf Jason B JB

Genetics 20181102 1

Genomic imprinting shapes the genotype-phenotype relationship by creating an asymmetry between the influences of paternally and maternally inherited gene copies. Consequently, imprinting can impact heritable and nonheritable variation, resemblance of relatives, and evolutionary dynamics. Although previous analyses have identified some of the quantitative genetic consequences of imprinting, we lack a framework that cleanly separates the influence of imprinting from other components of variation, ...[more]

PMID: 30389806

Similar Datasets

Project description: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.

Project description:1. There is a growing number of empirical reports of environmental change simultaneously influencing population dynamics, life history and quantitative characters. We do not have a well-developed understanding of links between the dynamics of these quantities. 2. Insight into the joint dynamics of populations, quantitative characters and life history can be gained by deriving a model that allows the calculation of fundamental quantities that underpin population ecology, evolutionary biology and life history. The parameterization and analysis of such a model for a specific system can be used to predict how a population will respond to environmental change. 3. Age-stage-structured models can be constructed from character-demography associations that describe age-specific relationships between the character and: (i) survival; (ii) fertility; (iii) ontogenetic development of the character among survivors; and (iv) the distribution of reproductive allocation. 4. These models can be used to calculate a wide range of useful biological quantities including population growth and structure; terms in the Price equation including selection differentials; estimates of biometric heritabilities; and life history descriptors including generation time. We showcase the method through parameterization of a model using data from a well-studied population of Soay sheep Ovis aries. 5. Perturbation analysis is used to investigate how the quantities listed in summary point 4 change as each parameter in each character-demography function is altered. 6. A wide range of joint dynamics of life history, quantitative characters and population growth can be generated in response to changes in different character-demography associations; we argue this explains the diversity of observations on the consequences of environmental change from studies of free-living populations. 7. The approach we describe has the potential to explain within and between species patterns in quantitative characters, life history and population dynamics.

Dataset Information

Evolutionary Quantitative Genetics of Genomic Imprinting.

Publications

Evolutionary Quantitative Genetics of Genomic Imprinting.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets