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Genome-wide relaxation and phylogenetic inertia of codon usage bias in the Neotropical Drosophila saltans species group


Authors:
Carolina Prediger 1,2; Erina A. Ferreira 2; David Ogereau 2; Amir Yassin 2; Lilian Madi-Ravazzi 2

Affiliations:
1) São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil; 2) Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), CNRS, IRD, Université Paris-Saclay, Gif-sur-Yvette, France

Keywords:
a. genome evolution; t. bioinformatic and genome tools

It is well established that Drosophila flies favor codons ending in C|G but relaxation in codon usage bias (CUB) pattern was reported for the willistoni and saltans groups, two Neotropical sister clades of the subgenus Sophophora. Those reports were, however, carried out with few genes (saltans group) or single genome (D. willistoni). Here, we generated whole genome sequences for 15 out of 23 species of the saltans group and evaluated CUB using a large set of genes in terms of the effective number of codons (ENC) and the relative synonymous codon usage (RSCU) index. We also investigated three forces that may be contributing to CUB, namely, mutational bias, selection pressure and drift. Our results indicated relaxation in CUB (mean ENC=48.33). Average RSCU index showed preference for codons ending in A|T. To evaluate mutational bias strength, we found moderate positive correlation between the RSCU of codons ending in G|C and the average G|C content at third position (GC3) for a given gene and a similarly moderate but negative correlation was seen for codons ending in A|T. Regarding translational selection, we found no correlation between tRNA adaptation index (stAI) and ENC after estimating tRNA diversity and content for four species for which genome assemblies have recently been published. We verified the strength of drift, by estimating the phylogenetic signal of RSCU on a phylogeny inferred from 30 genes, a heatmap with a hierarchical cluster analysis and a correspondence analysis. The first method indicated very strong phylogenetic signal for RSCU in the saltans group that was largely confirmed by the phylogenetic clustering of species by the second and third methods. In conclusion, our results demonstrate that relaxation of CUB in the saltans group is a general genome-wide pattern that has likely originated by mutational bias in the ancestor of the willistoni and saltans groups, and has since drifted along the evolutionary history of saltans species.