Evidence for Stabilizing Selection on Codon Usage in Chromosomal Rearrangements ofDrosophila 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.

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

“…Avoidance of the toxicity of misfolded proteins generated by translational errors has also been proposed as an explanation of CUB (Drummond and Wilke 2008). Recent work has also suggested the possibility that stabilizing, as opposed to directional, selection maintains the frequencies of synonymous codons, because CUB has been found to be unrelated to recombination rate in D. pseudoobscura , in line with theoretical predictions about the action of stabilizing selection (Charlesworth 2013; Fuller et al. 2014; Kliman 2014).…”

The role of chromosomal inversions in speciation

“…Chromosomal inversions can arise and persist in ancestral populations for long periods of time driven by selection in heterogeneous environments (41). During this period, the genomic regions spanning the inversions and the corresponding regions on the un-inverted chromosomes can accumulate genetic divergence aided by the suppression of recombination in heterozygotes (41)(42)(43)(44)(45).…”

Genomics of Natural Populations: Evolutionary Forces that Establish and Maintain Gene Arrangements inDrosophila pseudoosbscura

“…Genome sequences of 54 D. pseudoobscura strains were analyzed in this study. The genomes of 47 strains were described in the previous study of codon usage bias by Fuller et al (2014). The strains were collected from the seven localities: Mount Saint Helena, CA (MSH), Santa Cruz Island, CA (SCI) (collected by Luciano Matzkin, University of Arizona), James Reserve, CA (JR) (collected by Wyatt W. Anderson, University of Georgia), Kaibab National Forest, AZ (KB), Bosque del Apache Wild Life Refuge (BdA, collected by Sara Sheeley, Upper Iowa University and provided by Bryant McAllister, University of Iowa), Davis Mountains, TX (DM), and San Pablo Etla, Oaxaca, Mexico (SPE123) (collected by Theresa A. Markow, UC San Diego).…”