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Gene conflicts and the concepts of outlaw and sheriff alleles

1983; Academic Press; Volume: 6; Issue: 4 Linguagem: Inglês

10.1016/s0140-1750(83)90156-2

1878-2787

Steven J. Rothstein, David P. Barash,

Plant and animal studies

'Outlaw genes' are genetic units that favor themselves at the expense of the rest of the genome. Contrary to Alexander and Borgia (1978), who developed the outlaw concept, we suggest that outlawry will not be nullified consistently by the rest of the genome. Importantly, the kinds of outlaw alleles Alexander and Borgia consider must be associated with other gene loci either as a chromosome, gamete or organism and must then benefit, at least temporarily, other gene loci when they advance their own interests. We hypothesize the existence of 'sheriff alleles', which respond to outlawry and which are necessary to Alexander and Borgia's arguments. The optimal response that a potential sheriff allele could show to meiotic drive, a form of intragenomic outlawry, is to align consistently with the driver during meiosis rather than to suppress drive. A driving allele is easiest to detect if it is present at an intermediate frequency. Thus, detected cases of drive are probably an atypical subsample of all driving alleles because drivers should either be lost if they inflict large phenotypic defects or go to fixation, unless some complicated frequency-dependent process maintains them at intermediate levels. Within a population, selection will generally produce an equal sex ratio but outlaw X or Y chromosomes that have driving effects will be selected for. Maintenance of an equal sex ratio may be due to a stalemate of outlaw tendencies on both sex chromosomes, rather than to anti-outlaw actions of the autosomes. Intergenomic outlawry could operate if individuals carrying a specific allele deprive individuals who lack the allele of resources that they then use to increase their own fitness. The only situation in which the gene pool should 'favor' an end to intergenomic outlawry is that in which the overall benefits all alleles receive when carried by outlaw individuals do not compensate for the harm replicates of these alleles receive when carried by nonoutlaws. But even here, selection will favor sheriffs that operate selfishly by protecting only themselves from outlaws and allowing outlaws to harm alternative alleles at the sheriff's locus. Selfish sheriffs that increase to fixation could bring an end to observable outlawry but this process differs from the general genomic nullification and collective power proposed by Alexander and Borgia. Since both intra and intergenomic outlaws are most adaptive when they do not harm copies of themselves, an outlaw allele should be difficult to detect when present at a high frequency. Contrary to Alexander and Borgia, there is no reason to suppose that the genome is preadapted to counter outlaws as soon as they appear; and once outlaws become common, their nullification may provide little or no benefit to the genome. Thus, many alleles that are fixed or nearly so and that seem to be law abiding may have achieved their high frequency via outlawry.