Apomixis, a natural form of asexual seed production in plants, has evolved independently in various taxa, and represents an important potential technology for agriculture. The switch to apomixis is based on de-regulation of developmental pathways originally leading to sexual seed formation. Hybridization and polyploidy, both typical characteristics of asexual plants and animals, are mechanisms that could trigger de-regulation. Here we show that up-regulation of alleles in apomeiotic ovules is mediated by genomic duplication, heterochrony and the residual effects of ancient hybridization in diploid apomicts of the Boechera holboellii complex. Using SuperSAGE, we have identified over 4000 differentially expressed mRNA tags between micro-dissected ovules from two diploid sexual (Boechera stricta and B. holboellii) and two diploid apomictic (Boechera divaricarpa) accessions. Pairwise sequence comparisons between tags enabled identification of allelic variants of the same loci. Up-regulated candidate apomeiosis alleles consistently have more than three related alleles, thus demonstrating transcription from duplicated loci. A further 543 alleles were heterochronically expressed between sexual and apomeiotic ovules at developmental stages 2-II to 2-IV. Intriguingly, 69 B. holboellii specific alleles were preferentially up-regulated in apomeiotic ovules, thus showing a remnant‘parent of origin’ effect stemming from the Pleistocene origin of the hybrid B. divaricarpa from taxa related to B. holboellii and B. stricta. These data implicate polyploid gene dosage in the expression of asexual seed formation, and support hypotheses of de-regulation of the sexual pathway. The observed ‘parent of origin’ effect suggests that the genomic memory of hybridization has somehow been maintained after hundreds, if not thousands, of asexual generations.