In contrast to the two X chromosomes that participate equally in oogenic meiosis in mammals, during spermatogenesis the solitary X chromosome can be regarded as an inadequate pairing partner for the Y chromosome. Hence it is epigenetically silenced and consigned to the XY body. This silenced state can transfer between generations. The sleeping X will awake when in a female cell with an accompanying maternally donated X chromosome. Transgene experiments in nematodes indicate that a similar process can operate at the (...) level of chromosomal segments. A gene that mispairs at meiosis is epigenetically silenced and transferred to the next generation where its awakening is conditional on the presence of a meiotic pairing partner. These intergenerational transfers of epigenetic labelling, and intragenerational reversals thereof, might apply at the level of individual bases when confronted with inadequate pairing partners. During meiotic recombination, homologous DNA sequences of maternal and paternal origin pair to form a mutual duplex, and mismatches can be detected and corrected. But there is only a 50 % chance that the correction will favor a particular allele. There is information that a DNA duplex segment is in need of correction, but not how correction could asymmetrically favor one allele. If the segment were epigenetically marked as “suspect,” this information could be used in a future generation to favorably correct should more information, in the form of a homologous unmutated duplex, became available. So fundamental would this mechanism be that it would have provided a selection pressure for the emergence of epigenetic marking early in evolution. (shrink)