Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura

Zachary L. Fuller, Gwilym D. Haynes, Dianhui Zhu, Matthew Batterton, Hsu Chao, Shannon Dugan, Mehwish Javaid, Joy C. Jayaseelan, Sandra Lee, Mingmei Li, Fiona Ongeri, Sulan Qi, Yi Han, Harshavardhan Doddapaneni, Stephen Richards, Stephen Wade Schaeffer

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

There has been a renewed interest in investigating the role of stabilizing selection acting on genomewide traits such as codon usage bias. Codon bias, when synonymous codons are used at unequal frequencies, occurs in a wide variety of taxa. Standard evolutionary models explain the maintenance of codon bias through a balance of genetic drift, mutation and weak purifying selection. The efficacy of selection is expected to be reduced in regions of suppressed recombination. Contrary to observations in Drosophila melanogaster, some recent studies have failed to detect a relationship between the recombination rate, intensity of selection acting at synonymous sites, and the magnitude of codon bias as predicted under these standardmodels.Here, we examined codon bias in 2798 protein coding loci on the third chromosome of D. pseudoobscura using whole-genome sequences of 47 individuals, representing five common third chromosome gene arrangements. Fine-scale recombination maps were constructed using more than 1 million segregating sites. As expected, recombination was demonstrated to be significantly suppressed between chromosome arrangements, allowing for a direct examination of the relationship between recombination, selection, and codon bias. As with other Drosophila species, we observe a strong mutational bias away from the most frequently used codons. We find the rate of synonymous and nonsynonymous polymorphism is variable between different amino acids. However, we do not observe a reduction in codon bias or the strength of selection in regions of suppressed recombination as expected. Instead, we find that the interaction between weak stabilizing selection and mutational bias likely plays a role in shaping the composition of synonymous codons across the third chromosome in D. pseudoobscura.

Original languageEnglish (US)
Pages (from-to)2433-2449
Number of pages17
JournalG3: Genes, Genomes, Genetics
Volume4
Issue number12
DOIs
StatePublished - Jan 1 2014

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Codon
Drosophila
Genetic Recombination
Chromosomes, Human, 13-15
Selection Bias
Chromosomes
Genetic Drift
Gene Order
Drosophila melanogaster
Maintenance
Genome
Amino Acids
Mutation

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Genetics
  • Genetics(clinical)

Cite this

Fuller, Zachary L. ; Haynes, Gwilym D. ; Zhu, Dianhui ; Batterton, Matthew ; Chao, Hsu ; Dugan, Shannon ; Javaid, Mehwish ; Jayaseelan, Joy C. ; Lee, Sandra ; Li, Mingmei ; Ongeri, Fiona ; Qi, Sulan ; Han, Yi ; Doddapaneni, Harshavardhan ; Richards, Stephen ; Schaeffer, Stephen Wade. / Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura. In: G3: Genes, Genomes, Genetics. 2014 ; Vol. 4, No. 12. pp. 2433-2449.
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abstract = "There has been a renewed interest in investigating the role of stabilizing selection acting on genomewide traits such as codon usage bias. Codon bias, when synonymous codons are used at unequal frequencies, occurs in a wide variety of taxa. Standard evolutionary models explain the maintenance of codon bias through a balance of genetic drift, mutation and weak purifying selection. The efficacy of selection is expected to be reduced in regions of suppressed recombination. Contrary to observations in Drosophila melanogaster, some recent studies have failed to detect a relationship between the recombination rate, intensity of selection acting at synonymous sites, and the magnitude of codon bias as predicted under these standardmodels.Here, we examined codon bias in 2798 protein coding loci on the third chromosome of D. pseudoobscura using whole-genome sequences of 47 individuals, representing five common third chromosome gene arrangements. Fine-scale recombination maps were constructed using more than 1 million segregating sites. As expected, recombination was demonstrated to be significantly suppressed between chromosome arrangements, allowing for a direct examination of the relationship between recombination, selection, and codon bias. As with other Drosophila species, we observe a strong mutational bias away from the most frequently used codons. We find the rate of synonymous and nonsynonymous polymorphism is variable between different amino acids. However, we do not observe a reduction in codon bias or the strength of selection in regions of suppressed recombination as expected. Instead, we find that the interaction between weak stabilizing selection and mutational bias likely plays a role in shaping the composition of synonymous codons across the third chromosome in D. pseudoobscura.",
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Fuller, ZL, Haynes, GD, Zhu, D, Batterton, M, Chao, H, Dugan, S, Javaid, M, Jayaseelan, JC, Lee, S, Li, M, Ongeri, F, Qi, S, Han, Y, Doddapaneni, H, Richards, S & Schaeffer, SW 2014, 'Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura', G3: Genes, Genomes, Genetics, vol. 4, no. 12, pp. 2433-2449. https://doi.org/10.1534/g3.114.014860

Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura. / Fuller, Zachary L.; Haynes, Gwilym D.; Zhu, Dianhui; Batterton, Matthew; Chao, Hsu; Dugan, Shannon; Javaid, Mehwish; Jayaseelan, Joy C.; Lee, Sandra; Li, Mingmei; Ongeri, Fiona; Qi, Sulan; Han, Yi; Doddapaneni, Harshavardhan; Richards, Stephen; Schaeffer, Stephen Wade.

In: G3: Genes, Genomes, Genetics, Vol. 4, No. 12, 01.01.2014, p. 2433-2449.

Research output: Contribution to journalArticle

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T1 - Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura

AU - Fuller, Zachary L.

AU - Haynes, Gwilym D.

AU - Zhu, Dianhui

AU - Batterton, Matthew

AU - Chao, Hsu

AU - Dugan, Shannon

AU - Javaid, Mehwish

AU - Jayaseelan, Joy C.

AU - Lee, Sandra

AU - Li, Mingmei

AU - Ongeri, Fiona

AU - Qi, Sulan

AU - Han, Yi

AU - Doddapaneni, Harshavardhan

AU - Richards, Stephen

AU - Schaeffer, Stephen Wade

PY - 2014/1/1

Y1 - 2014/1/1

N2 - There has been a renewed interest in investigating the role of stabilizing selection acting on genomewide traits such as codon usage bias. Codon bias, when synonymous codons are used at unequal frequencies, occurs in a wide variety of taxa. Standard evolutionary models explain the maintenance of codon bias through a balance of genetic drift, mutation and weak purifying selection. The efficacy of selection is expected to be reduced in regions of suppressed recombination. Contrary to observations in Drosophila melanogaster, some recent studies have failed to detect a relationship between the recombination rate, intensity of selection acting at synonymous sites, and the magnitude of codon bias as predicted under these standardmodels.Here, we examined codon bias in 2798 protein coding loci on the third chromosome of D. pseudoobscura using whole-genome sequences of 47 individuals, representing five common third chromosome gene arrangements. Fine-scale recombination maps were constructed using more than 1 million segregating sites. As expected, recombination was demonstrated to be significantly suppressed between chromosome arrangements, allowing for a direct examination of the relationship between recombination, selection, and codon bias. As with other Drosophila species, we observe a strong mutational bias away from the most frequently used codons. We find the rate of synonymous and nonsynonymous polymorphism is variable between different amino acids. However, we do not observe a reduction in codon bias or the strength of selection in regions of suppressed recombination as expected. Instead, we find that the interaction between weak stabilizing selection and mutational bias likely plays a role in shaping the composition of synonymous codons across the third chromosome in D. pseudoobscura.

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