Abstract

BackgroundAlthough mitochondrial (mt) gene order is highly conserved among vertebrates, widespread gene rearrangements occur in anurans, especially in neobatrachians. Protein coding genes in the mitogenome experience adaptive or purifying selection, yet the role that selection plays on genomic reorganization remains unclear. We sequence the mitogenomes of three species of Glandirana and hot spots of gene rearrangements of 20 frog species to investigate the diversity of mitogenomic reorganization in the Neobatrachia. By combing these data with other mitogenomes in GenBank, we evaluate if selective pressures or functional constraints act on mitogenomic reorganization in the Neobatrachia. We also look for correlations between tRNA positions and codon usage.ResultsGene organization in Glandirana was typical of neobatrachian mitogenomes except for the presence of pseudogene trnS (AGY). Surveyed ranids largely exhibited gene arrangements typical of neobatrachian mtDNA although some gene rearrangements occurred. The correlation between codon usage and tRNA positions in neobatrachians was weak, and did not increase after identifying recurrent rearrangements as revealed by basal neobatrachians. Codon usage and tRNA positions were not significantly correlated when considering tRNA gene duplications or losses. Change in number of tRNA gene copies, which was driven by genomic reorganization, did not influence codon usage bias. Nucleotide substitution rates and dN/dS ratios were higher in neobatrachian mitogenomes than in archaeobatrachians, but the rates of mitogenomic reorganization and mt nucleotide diversity were not significantly correlated.ConclusionsNo evidence suggests that adaptive selection drove the reorganization of neobatrachian mitogenomes. In contrast, protein-coding genes that function in metabolism showed evidence for purifying selection, and some functional constraints appear to act on the organization of rRNA and tRNA genes. As important nonadaptive forces, genetic drift and mutation pressure may drive the fixation and evolution of mitogenomic reorganizations.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-691) contains supplementary material, which is available to authorized users.

Highlights

  • Mitochondrial gene order is highly conserved among vertebrates, widespread gene rearrangements occur in anurans, especially in neobatrachians

  • Evidence for adaptive evolution of mitochondrial DNA (mtDNA) genes exists in some vertebrate lineages, such as mammals and reptiles [7,8,9]

  • The genomic duplication is more likely to occur in lineages where the efficiency of selection had been reduced and the ratio of nonsynonymous to synonymous substitution increased. These findings indicate that mitogenomic reorganization accompanies lower or relaxed selection, and that fixation of the structural alteration is nonadaptive [11,12]

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Summary

Introduction

Mitochondrial (mt) gene order is highly conserved among vertebrates, widespread gene rearrangements occur in anurans, especially in neobatrachians. We sequence the mitogenomes of three species of Glandirana and hot spots of gene rearrangements of 20 frog species to investigate the diversity of mitogenomic reorganization in the Neobatrachia. The mitogenome of metazoans encodes 13 protein-coding genes along with 2 rRNAs and 22 tRNAs. The 13 protein-coding genes, all of which play vital roles in the respiration chain, producing 95% of the adenosine triphosphate (ATP) required for cellular energy through oxidative phosphorylation [5]. The 13 protein-coding genes, all of which play vital roles in the respiration chain, producing 95% of the adenosine triphosphate (ATP) required for cellular energy through oxidative phosphorylation [5] The function of these proteins results in the distribution of mitochondrial DNA (mtDNA) diversity being far from random [6]. Evidence for adaptive evolution of mtDNA genes exists in some vertebrate lineages, such as mammals and reptiles [7,8,9]

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