Population Genomic Analysis Reveals No Evidence for GC-Biased Gene Conversion in Drosophila melanogaster

Robinson, Matthew C.; Stone, Eric A.; Singh, Nadia D.

doi:10.1093/molbev/mst220

Cited by 42 publications

(48 citation statements)

References 65 publications

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“…2010), and are thought to be closer to base composition equilibrium than other genomic regions (Kern and Begun 2005; Haddrill and Charlesworth 2008; Singh et al. 2009; Robinson et al. 2014), a pattern we have also observed (fig.…”

Section: Discussionmentioning

confidence: 99%

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Variation in the intensity of selection on codon bias over time causes contrasting patterns of base composition evolution in Drosophila

et al. 2017

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Four-fold degenerate coding sites form a major component of the genome, and are often used to make inferences about selection and demography, so that understanding their evolution is important. Despite previous efforts, many questions regarding the causes of base composition changes at these sites in Drosophila remain unanswered. To shed further light on this issue, we obtained a new whole-genome polymorphism data set from D. simulans. We analyzed samples from the putatively ancestral range of D. simulans, as well as an existing polymorphism data set from an African population of D. melanogaster. By using D. yakuba as an outgroup, we found clear evidence for selection on 4-fold sites along both lineages over a substantial period, with the intensity of selection increasing with GC content. Based on an explicit model of base composition evolution, we suggest that the observed AT-biased substitution pattern in both lineages is probably due to an ancestral reduction in selection intensity, and is unlikely to be the result of an increase in mutational bias towards AT alone. By using two polymorphism-based methods for estimating selection coefficients over different timescales, we show that the selection intensity on codon usage has been rather stable in D. simulans in the recent past, but the long-term estimates in D. melanogaster are much higher than the short-term ones, indicating a continuing decline in selection intensity, to such an extent that the short-term estimates suggest that selection is only active in the most GC-rich parts of the genome. Finally, we provide evidence for complex evolutionary patterns in the putatively neutral short introns, which cannot be explained by the standard GC-biased gene conversion model. These results reveal a dynamic picture of base composition evolution.

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Section: Discussionmentioning

confidence: 99%

“…2012; Campos et al. 2013; Robinson et al. 2014), although there is some evidence either for the action of selection for GC basepairs or gBGC on the evolution of non-coding sequences in D. simulans (Haddrill and Charlesworth 2008).…”

Section: Introductionmentioning

confidence: 99%

Variation in the intensity of selection on codon bias over time causes contrasting patterns of base composition evolution in Drosophila

et al. 2017

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show abstract

Section: Discussionmentioning

confidence: 99%

“…Although several studies have supported significant gcBGC effects in Drosophila (Marais et al 2001; Singh et al 2005b; Haddrill and Charlesworth 2008) recent studies based on whole genome level recombination rates and polymorphisms from D. melanogaster have suggested otherwise (Comeron et al 2012; Robinson et al 2014). Robinson et al (2014) has suggested the different amount of gcBGC between the X chromosome and autosomes could be due to a shift in the mutational processes. Here, analysis of short introns from the X chromosome and autosomes of D. ananassae , which were previously shown to be close to neutrality in Drosophila (Haddrill et al 2005; Halligan and Keightley 2006; Singh et al 2009; Robinson et al 2014), would indicate any potential difference in the mutational process.…”

Section: Discussionmentioning

confidence: 99%

“…Robinson et al (2014) has suggested the different amount of gcBGC between the X chromosome and autosomes could be due to a shift in the mutational processes. Here, analysis of short introns from the X chromosome and autosomes of D. ananassae , which were previously shown to be close to neutrality in Drosophila (Haddrill et al 2005; Halligan and Keightley 2006; Singh et al 2009; Robinson et al 2014), would indicate any potential difference in the mutational process.…”

Section: Discussionmentioning

confidence: 99%

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Recent and Long-Term Selection Across Synonymous Sites in Drosophila ananassae

Choi

Aquadro

2016

J Mol Evol

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In Drosophila, many studies have examined the short or long term evolution occurring across synonymous sites. Few, however, have examined both the recent and long-term evolution to gain a complete view of this selection. Here we have analyzed Drosophila ananassae DNA polymorphism and divergence data using several different methods, and have identified evidence of positive selection favoring preferred codons in both recent and long-term evolutionary time scale. Further in D. ananassae, the strength of selection for preferred codons was stronger on the X chromosome compared to the autosomes. We show that this stronger selection is not due to higher gene expression of X linked genes. Analysis of the selectively neutral introns indicated the X chromosome also had a preference for GC over AT nucleotides, potentially from GC biased gene conversions (gcBGC) that can also affect the base composition of synonymous sites. Thus selection for preferred codons and gcBGC both seem to be partially responsible for shaping the D. ananassae synonymous site evolution.

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GC‐biased gene conversion links the recombination landscape and demography to genomic base composition

Mugal

Weber²,

Ellegren

2015

BioEssays

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The origin and evolutionary dynamics of the spatial heterogeneity in genomic base composition have been debated since its discovery in the 1970s. With the recent availability of numerous genome sequences from a wide range of species it has been possible to address this question from a comparative perspective, and similarities and differences in base composition between groups of organisms are becoming evident. Ample evidence suggests that the contrasting dynamics of base composition are driven by GC-biased gene conversion (gBGC), a process that is associated with meiotic recombination. In line with this hypothesis, base composition is associated with the rate of recombination and the evolutionary dynamics of the recombination landscape, therefore, governs base composition. In addition, and at first sight perhaps surprisingly, the relationship between demography and genomic base composition is in agreement with the gBGC hypothesis: organisms with larger populations have higher GC content than those with smaller populations.

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Population Genomic Analysis Reveals No Evidence for GC-Biased Gene Conversion in Drosophila melanogaster

Cited by 42 publications

References 65 publications

Variation in the intensity of selection on codon bias over time causes contrasting patterns of base composition evolution in Drosophila

Variation in the intensity of selection on codon bias over time causes contrasting patterns of base composition evolution in Drosophila

Recent and Long-Term Selection Across Synonymous Sites in Drosophila ananassae

GC‐biased gene conversion links the recombination landscape and demography to genomic base composition

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