Sightings of the revolutionary comet that appeared in the skies of evolutionary biology in 1976—the selfish gene—date back to the 19th and early 20th centuries. It became generally recognized that genes were located on chromosomes and compete with each other in a manner consistent with the later appellation “selfish.” Chromosomes were seen as disruptable by the apparently random “cut and paste” process known as recombination. However, each gene was only a small part of its chromosome. On a statistical basis a (...) gene should escape disruption for many generations. This led George Williams and Richard Dawkins to a new definition of the gene, differing from conventional biochemical definitions in that there were no consistent genic boundaries. There had been no previous sightings of another revolutionary, albeit less verbally spectacular, comet that appeared in 1975—the homostability principle of Akiyoshi Wada. Each gene has a base composition “accent” that distinguishes it from its neighbors. We now see that recombination can be triggered by the shift in base composition at genic boundaries. Hence, the Williams-Dawkins definition approaches the conventional definitions. (shrink)

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)

Four years after the death of Charles Darwin, his research associate, George Romanes, invoked a mysterious process—“physiological selection”—that could often have secured reproductive isolation independently of, and prior to, natural selection, so leading to an origin of species. This postulate of two sequential selection modes can now be regarded as leading to modern “chromosomal,” as opposed to “genic,” speciation theories. Romanes’ abstractions—which confounded many, but not all, of his contemporaries—equate with divergences in parental DNA sequences that impede meiotic pairing in (...) their hybrid offspring, so rendering that offspring sterile. Unlike Darwin, Romanes saw hybrid sterility as a parental, rather than offspring, phenotype that would, within a species, reproductively isolate certain parents from each other while not impeding their crossing with other parents. This group selection would have empowered natural selection to act more advantageously than in its absence. Given suitable conditions, there could then be divergence from one species into two. The present essay introduces Romanes’ “Physiological Selection; an Additional Suggestion on the Origin of Species” 19:337–411; available as supplementary material in the online version of this essay) for the journal’s “Classics in Biological Theory” collection. (shrink)