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A simple expression for the strength of selection on recombination generated by interference among mutations.

ABSTRACT: One of the most widely cited hypotheses to explain the evolutionary maintenance of genetic recombination states that the reshuffling of genotypes at meiosis increases the efficiency of natural selection by reducing interference among selected loci. However, and despite several decades of theoretical work, a quantitative estimation of the possible selective advantage of a mutant allele increasing chromosomal map length (the average number of cross-overs at meiosis) remains difficult. This article derives a simple expression for the strength of selection acting on a modifier gene affecting the genetic map length of a whole chromosome or genome undergoing recurrent mutation. In particular, it shows that indirect selection for recombination caused by interference among mutations is proportional to [Formula: see text], where [Formula: see text] is the effective population size, U is the deleterious mutation rate per chromosome, and R is the chromosome map length. Indirect selection is relatively insensitive to the fitness effects of deleterious alleles, epistasis, or the genetic architecture of recombination rate variation and may compensate for substantial costs associated with recombination when linkage is tight. However, its effect generally stays weak in large, highly recombining populations.

SUBMITTER: Roze D

PROVIDER: S-EPMC8126786 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Free-living bacteria are usually thought to have large effective population sizes, and so tiny selective differences can drive their evolution. However, because recombination is infrequent, "background selection" against slightly deleterious alleles should reduce the effective population size (Ne) by orders of magnitude. For example, for a well-mixed population with 10(12) individuals and a typical level of homologous recombination (r/m = 3, i.e., nucleotide changes due to recombination [r] occur at 3 times the mutation rate [m]), we predict that Ne is <10(7). An argument for high Ne values for bacteria has been the high genetic diversity within many bacterial "species," but this diversity may be due to population structure: diversity across subpopulations can be far higher than diversity within a subpopulation, which makes it difficult to estimate Ne correctly. Given an estimate of Ne, standard population genetics models imply that selection should be sufficient to drive evolution if Ne × s is >1, where s is the selection coefficient. We found that this remains approximately correct if background selection is occurring or when population structure is present. Overall, we predict that even for free-living bacteria with enormous populations, natural selection is only a significant force if s is above 10(-7) or so.Because bacteria form huge populations with trillions of individuals, the simplest theoretical prediction is that the better allele at a site would predominate even if its advantage was just 10(-9) per generation. In other words, virtually every nucleotide would be at the local optimum in most individuals. A more sophisticated theory considers that bacterial genomes have millions of sites each and selection events on these many sites could interfere with each other, so that only larger effects would be important. However, bacteria can exchange genetic material, and in principle, this exchange could eliminate the interference between the evolution of the sites. We used simulations to confirm that during multisite evolution with realistic levels of recombination, only larger effects are important. We propose that advantages of less than 10(-7) are effectively neutral.

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A simple expression for the strength of selection on recombination generated by interference among mutations.

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