Natural selection and the function of genome imprinting: beyond the silenced minority

Most hypotheses of the evolutionary origin of genome imprinting assume that the biochemical character an which natural selection has operated is the e xpression of the allele from only one parent at an affected locus. We propo se an alternative - that natural selection has operated on differences in t he chromatin structure of maternal and paternal chromosomes to facilitate p airing during meiosis and to maintain the distinction between homologues du ring DNA repair and recombination in both meiotic and mitotic cells. Mainte nance of differences in chromatin structure in somatic cells can sometimes result in the transcription of only one allele at a locus. This pattern of transcription might be selected, in same instances, for reasons that are un related to the original establishment of the imprint. Differences in the ch romatin structure of homologous chromosomes might facilitate pairing and re combination during meiosis, but some such differences could also result in non-random segregation of chromosomes, leading to parental-origin-dependent transmission ratio distortion. This hypothesis unites two broad classes of parental origin effects under a single selective force and identifies a si ngle substrate through which Mendel's first and second laws might be violat ed.