Hill–Robertson interference in <i>Drosophila melanogaster</i>: reply to Marais, Mouchiroud and Duret

Kliman, Richard M.; Hey, Jody

doi:10.1017/s0016672302006067

Cited by 40 publications

(33 citation statements)

References 8 publications

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“…nation (see Materials and Methods) are also negatively correlated with recombination rate, six of them significantly so (Kendall's s £ )0.05, p £ 0.03 for ACE, HK-p, CC99, KH93, CK00, MMDO1). It has been previously noted that the relationship between codon bias and recombination rate is nonlinear, and that there appears to be a recombination threshold (of 2cM/Mbp) above which the positive relationship between these two factors no longer holds (Kliman and Hey 2003). Though our recombination categories do not delineate genomic regions precisely above and below the suggested threshold, our data do hint at the possibility that the relationship between codon bias and recombination rate is indeed non-linear (Fig.…”

Section: Codon Usage and Recombination Ratementioning

confidence: 40%

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

2005

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Abstract. The patterns and processes of molecular evolution may differ between the X chromosome and the autosomes in Drosophila melanogaster. This may in part be due to differences in the effective population size between the two chromosome sets and in part to the hemizygosity of the X chromosome in Drosophila males. These and other factors may lead to differences both in the gene complements of the X and the autosomes and in the properties of the genes residing on those chromosomes. Here we show that codon bias and recombination rate are correlated strongly and negatively on the X chromosome, and that this correlation cannot be explained by indirect relationships with other known determinants of codon bias. This is in dramatic contrast to the weak positive correlation found on the autosomes. We explored possible explanations for these patterns, which required a comprehensive analysis of the relationships among multiple genetic properties such as protein length and expression level. This analysis highlights conserved features of coding sequence evolution on the X and the autosomes and illuminates interesting differences between these two chromosome sets.

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Section: Codon Usage and Recombination Ratementioning

confidence: 40%

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

2005

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“…In addition, the potential influences of biased gene conversion (Marais et al 2001Kliman and Hey 2003;Marais 2003), changes in the recombinational landscape (Takano-Shimizu 1999), and recent changes in the mutational processes (Takano-Shimizu 2001;Kern and Begun 2005), as well as the effects of more complex demographic models (e.g., population structure and population bottlenecks), are not considered by our method. Therefore, although there is evidence for selection on synonymous sites, this result should be treated with caution.…”

Section: Discussionmentioning

confidence: 99%

Estimating Selection Intensity on Synonymous Codon Usage in a Nonequilibrium Population

2009

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Codon usage bias is the nonrandom use of synonymous codons for the same amino acid. Most population genetic models of codon usage evolution assume that the population is at mutation-selection-drift equilibrium. Natural populations, however, frequently deviate from equilibrium, often because of recent demographic changes. Here, we construct a matrix model that includes the effects of a recent change in population size on estimates of selection on preferred vs. unpreferred codons. Our results suggest that patterns of synonymous polymorphisms affecting codon usage can be quite erratic after such a change; statistical methods that fail to take demographic effects into account can then give incorrect estimates of important parameters. We propose a new method that can accurately estimate both demographic and codon usage parameters. The method also provides a simple way of testing for the effects of covariates such as gene length and level of gene expression on the intensity of selection, which we apply to a large Drosophila melanogaster polymorphism data set. Our analyses of twofold degenerate codons reveal that (i) selection acts in favor of preferred codons, (ii) there is mutational bias in favor of unpreferred codons, (iii) shorter genes and genes with higher expression levels are under stronger selection, and (iv) there is little evidence for a recent change in population size in the Zimbabwe population of D. melanogaster. CODONS specifying the same amino acid are called synonymous codons. These are often used nonrandomly, with some codons appearing more frequently than others. This biased usage of synonymous codons has been found in many organisms such as Drosophila, yeast, and bacteria (Ikemura 1985;Duret and Mouchiroud 1999;Hershberg and Petrov 2008). Conventionally, synonymous codons for a given amino acid are divided into two classes: preferred and unpreferred codons (Ikemura 1985;Akashi 1994;Duret and Mouchiroud 1999). Several observations indicate that codon usage is affected by natural selection. First, in species with codon usage bias, preferred codons generally correspond to the most abundant tRNA species (Ikemura 1981). Second, highly expressed genes usually have higher codon usage bias than genes with low expression (Sharp and Li 1986;Duret and Mouchiroud 1999;Hey and Kliman 2002). Third, the synonymous substitution rate of a gene has been shown to be negatively correlated with its degree of codon usage bias (Sharp and Li 1986;Bierne and Eyre-Walker 2006). The most commonly cited explanations of the apparent fitness differences between preferred and unpreferred codons are selection for translation efficiency, translational accuracy, and mRNA stability (Ikemura 1985;Eyre-Walker and Bulmer 1993;Akashi 1994;Drummond et al. 2005). Recently, it has been proposed that exon splicing also affects codon usage bias (Warnecke and Hurst 2007).From a population genetics perspective, the extent of codon usage bias is ultimately a product of the joint effects of mutation, selection, genetic drift, recombinati...

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“…For instance, biased resolution of heteroduplex DNA that arises during crossover may have evolutionary effects that mimic weak selection (Nagylaki, 1983). In some eukaryotes heteroduplex DNA appears to be biased toward resolution as a GC base pair (that is, GC-biased gene conversion) and one could propose that the same bias might occur in Drosophila, explaining a positive relationship between recombination rate and use of preferred (G-and C-ending) codons (Marais et al, 2001(Marais et al, , 2003Marais and Piganeau, 2002;Kliman and Hey, 2003a). Nevertheless, a GC-biased gene conversion model (Nagylaki, 1983) predicts that noncoding regions would show (1) a continuous increase in G þ C content with recombination and (2) a reduction in rates of evolution in genomic regions with high recombination and G þ C content.…”

Section: Direct and Indirect Evidence Of Hr In Eukaryotesmentioning

confidence: 99%

The Hill–Robertson effect: evolutionary consequences of weak selection and linkage in finite populations

2007

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The 'Hill-Robertson (HR) effect' describes that linkage between sites under selection will reduce the overall effectiveness of selection in finite populations. Here we discuss the major concepts associated with the HR effect and present results of computer simulations focusing on the linkage effects generated by multiple sites under weak selection. Most models of linkage and selection forecast differences in effectiveness of selection between chromosomes or chromosomal regions involving a number of genes. The abundance and physical clustering of weakly selected mutations across genomes, however, justify the investigation of HR effects at a very local level and we pay particular attention to linkage effects among selected sites of the same gene. Overall, HR effects caused by weakly selected mutations predict differences in effectiveness of selection between genes that differ in exon-intron structures and across genes. Under this scenario, introns might play an advantageous role reducing intragenic HR effects. Finally, we summarize observations that are consistent with local HR effects in Drosophila, discuss potential consequences on population genetic studies and suggest future lines of research.

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Hill–Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret

Cited by 40 publications

References 8 publications

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

Estimating Selection Intensity on Synonymous Codon Usage in a Nonequilibrium Population

The Hill–Robertson effect: evolutionary consequences of weak selection and linkage in finite populations

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