Independent origin of genomic imprinting in placental fish

Genomic imprinting results in biased expression of one parental allele. Such non-Mendelian expression occurs in angiosperms and placental mammals, which share having an active paternal genome during maternal offspring provisioning. It is hypothesized that imprinting modulates conflict between maternal control of resource allocation and paternal control of resource acquisition. If true, then imprinting should evolve in any organism that evolves a placenta. Here, we demonstrate genomic imprinting in a placental poeciliid fish, Poeciliopsis prolifica . Using transcriptomes from reciprocal crosses between two inbred strains, we identified 84 protein-coding genes with robust evidence of imprinting in P. prolifica placenta. These include the teleost ortholog of mammalian imprinted gene, grb10 , and a pair of adjacent genes, dpp4 and gcga , with opposing effects on glucose metabolism that are oppositely imprinted in a fashion that potentially resolves parental conflict. Significantly elevated allelic DNA methylation on the promoters of two focal imprinted genes suggests epigenetic mechanisms of imprinting similar to those in mammals. We also discovered the convergent recruitment of a gene network associated with nutrient transport in mammals. To our knowledge, this is the first demonstration of genomic imprinting in a non-mammalian vertebrate and supports the potential role of imprinting in resolving parental conflict.