Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster

Codon usage bias (CUB) in Drosophila is higher for X-linked genes than for autosomal genes. One possible explanation is that the higher effective recombination rate for genes on the X chromosome compared with the autosomes reduces their susceptibility to Hill–Robertson effects, and thus enhances the...

Full description

Bibliographic Details
Main Authors: Campos, Jose L., Zeng, Kai, Parker, Darren J., Charlesworth, Brian, Haddrill, Penelope R.
Format: Online
Language:English
Published: Oxford University Press 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3603305/
id pubmed-3603305
recordtype oai_dc
spelling pubmed-36033052013-03-20 Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster Campos, Jose L. Zeng, Kai Parker, Darren J. Charlesworth, Brian Haddrill, Penelope R. Discoveries Codon usage bias (CUB) in Drosophila is higher for X-linked genes than for autosomal genes. One possible explanation is that the higher effective recombination rate for genes on the X chromosome compared with the autosomes reduces their susceptibility to Hill–Robertson effects, and thus enhances the efficacy of selection on codon usage. The genome sequence of D. melanogaster was used to test this hypothesis. Contrary to expectation, it was found that, after correcting for the effective recombination rate, CUB remained higher on the X than on the autosomes. In contrast, an analysis of polymorphism data from a Rwandan population showed that mean nucleotide site diversity at 4-fold degenerate sites for genes on the X is approximately three-quarters of the autosomal value after correcting for the effective recombination rate, compared with approximate equality before correction. In addition, these data show that selection for preferred versus unpreferred synonymous variants is stronger on the X than the autosomes, which accounts for the higher CUB of genes on the X chromosome. This difference in the strength of selection does not appear to reflect the effects of dominance of mutations affecting codon usage, differences in gene expression levels between X and autosomes, or differences in mutational bias. Its cause therefore remains unexplained. The stronger selection on CUB on the X chromosome leads to a lower rate of synonymous site divergence compared with the autosomes; this will cause a stronger upward bias for X than A in estimates of the proportion of nonsynonymous mutations fixed by positive selection, for methods based on the McDonald–Kreitman test. Oxford University Press 2013-04 2012-11-29 /pmc/articles/PMC3603305/ /pubmed/23204387 http://dx.doi.org/10.1093/molbev/mss222 Text en © The Author(s) 2012. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Campos, Jose L.
Zeng, Kai
Parker, Darren J.
Charlesworth, Brian
Haddrill, Penelope R.
spellingShingle Campos, Jose L.
Zeng, Kai
Parker, Darren J.
Charlesworth, Brian
Haddrill, Penelope R.
Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster
author_facet Campos, Jose L.
Zeng, Kai
Parker, Darren J.
Charlesworth, Brian
Haddrill, Penelope R.
author_sort Campos, Jose L.
title Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster
title_short Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster
title_full Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster
title_fullStr Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster
title_full_unstemmed Codon Usage Bias and Effective Population Sizes on the X Chromosome versus the Autosomes in Drosophila melanogaster
title_sort codon usage bias and effective population sizes on the x chromosome versus the autosomes in drosophila melanogaster
description Codon usage bias (CUB) in Drosophila is higher for X-linked genes than for autosomal genes. One possible explanation is that the higher effective recombination rate for genes on the X chromosome compared with the autosomes reduces their susceptibility to Hill–Robertson effects, and thus enhances the efficacy of selection on codon usage. The genome sequence of D. melanogaster was used to test this hypothesis. Contrary to expectation, it was found that, after correcting for the effective recombination rate, CUB remained higher on the X than on the autosomes. In contrast, an analysis of polymorphism data from a Rwandan population showed that mean nucleotide site diversity at 4-fold degenerate sites for genes on the X is approximately three-quarters of the autosomal value after correcting for the effective recombination rate, compared with approximate equality before correction. In addition, these data show that selection for preferred versus unpreferred synonymous variants is stronger on the X than the autosomes, which accounts for the higher CUB of genes on the X chromosome. This difference in the strength of selection does not appear to reflect the effects of dominance of mutations affecting codon usage, differences in gene expression levels between X and autosomes, or differences in mutational bias. Its cause therefore remains unexplained. The stronger selection on CUB on the X chromosome leads to a lower rate of synonymous site divergence compared with the autosomes; this will cause a stronger upward bias for X than A in estimates of the proportion of nonsynonymous mutations fixed by positive selection, for methods based on the McDonald–Kreitman test.
publisher Oxford University Press
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3603305/
_version_ 1611964090302857216