title: Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura.
abstract: There has been a renewed interest in investigating the role of stabilizing selection acting on genome-wide 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 standard models. 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.
authors.affiliation: Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802-5301 zlf105@psu.edu.
authors.forename: Zachary L
authors.identifier: http://orcid.org/0000-0003-4765-9227
authors.initials: ZL
authors.lastname: Fuller
authors.affiliation: Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802-5301.
authors.forename: Gwilym D
authors.initials: GD
authors.lastname: Haynes
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Dianhui
authors.initials: D
authors.lastname: Zhu
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Matthew
authors.initials: M
authors.lastname: Batterton
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Hsu
authors.initials: H
authors.lastname: Chao
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Shannon
authors.initials: S
authors.lastname: Dugan
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Mehwish
authors.initials: M
authors.lastname: Javaid
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Joy C
authors.initials: JC
authors.lastname: Jayaseelan
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Sandra
authors.initials: S
authors.lastname: Lee
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Mingmei
authors.initials: M
authors.lastname: Li
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Fiona
authors.initials: F
authors.lastname: Ongeri
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Sulan
authors.initials: S
authors.lastname: Qi
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Yi
authors.initials: Y
authors.lastname: Han
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Harshavardhan
authors.initials: H
authors.lastname: Doddapaneni
authors.affiliation: Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030.
authors.forename: Stephen
authors.initials: S
authors.lastname: Richards
authors.affiliation: Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802-5301.
authors.forename: Stephen W
authors.initials: SW
authors.lastname: Schaeffer
mesh_terms: D000818:Animals; D002875:Chromosomes / Q000235:genetics*; D003062:Codon; D004330:Drosophila / Q000235:genetics*; D059014:High-Throughput Nucleotide Sequencing; D020641:Polymorphism, Single Nucleotide; D011995:Recombination, Genetic; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA
chemical_list: D003062:Codon
keywords: chromosomal inversions; codon bias; recombination; stabilizing selection