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

Benjamin C. Jackson, José L. Campos, Penelope R. Haddrill, Brian Charlesworth, Kai Zeng

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

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.
LanguageEnglish
Pages102-123
Number of pages22
JournalGenome Biology and Evolution
Volume9
Issue number1
DOIs
Publication statusPublished - 12 Jan 2017

Fingerprint

selection intensity
Base Composition
codons
Codon
Drosophila
Melanogaster
genetic polymorphism
genome
Genome Components
Genome
Gene Conversion
Drosophila simulans
polymorphism
gene conversion
selection methods
demography
Introns
introns
Demography
fold

Keywords

  • codon usage bias
  • nonequilibrium behaviour
  • selection
  • short introns
  • nonequilibrium behavior
  • Drosophila
  • evolution
  • genome

Cite this

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abstract = "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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Variation in the intensity of selection on codon bias over time causes contrasting patterns of base composition evolution in Drosophila. / Jackson, Benjamin C.; Campos, José L.; Haddrill, Penelope R.; Charlesworth, Brian; Zeng, Kai.

In: Genome Biology and Evolution, Vol. 9, No. 1, 12.01.2017, p. 102-123.

Research output: Contribution to journalArticle

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AU - Zeng, Kai

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