Genomic imprinting is the differential expression of an allele based on the parent of origin. Recent transcriptome-wide evaluations of the number of imprinted genes reveal complex patterns of imprinted expression among developmental stages and cell types. Such data demand a comprehensive evolutionary framework in which to understand the effect of natural selection on imprinted gene expression. We present such a framework for how asymmetries in demographic parameters and fitness effects can lead to the evolution of genomic imprinting and place recent theoretical advances in this framework. This represents a modern interpretation of the kinship theory, is well suited to studying populations with complex social interactions, and provides predictions which can be tested with forthcoming transcriptomic data. To understand the intricate phenotypic patterns that are emerging from the recent deluge of data, future investigations of genomic imprinting will require integrating evolutionary theory, transcriptomic data, developmental and functional genetics, and natural history.
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We thank Graham Coop and Stephanie Kamel for helpful comments on the manuscript. The Santa Fe Institute provided travel funds for a working group devoted to developing the ideas presented here. J.V. acknowledges support from an Omiydar Postdoctoral Fellowship at the Santa Fe Institute and Y.B. support from the National Science Foundation Bioinformatics Postdoctoral Fellowship Program.