Abstract
BackgroundMitochondrial genomic (mitogenomic) reorganizations are rarely found in closely-related animals, yet drastic reorganizations have been found in the Ranoides frogs. The phylogenetic relationships of the three major ranoid taxa (Natatanura, Microhylidae, and Afrobatrachia) have been problematic, and mitogenomic information for afrobatrachians has not been available. Several molecular models for mitochondrial (mt) gene rearrangements have been proposed, but observational evidence has been insufficient to evaluate them. Furthermore, evolutionary trends in rearranged mt genes have not been well understood. To gain molecular and phylogenetic insights into these issues, we analyzed the mt genomes of four afrobatrachian species (Breviceps adspersus, Hemisus marmoratus, Hyperolius marmoratus, and Trichobatrachus robustus) and performed molecular phylogenetic analyses. Furthermore we searched for two evolutionary patterns expected in the rearranged mt genes of ranoids.ResultsExtensively reorganized mt genomes having many duplicated and rearranged genes were found in three of the four afrobatrachians analyzed. In fact, Breviceps has the largest known mt genome among vertebrates. Although the kinds of duplicated and rearranged genes differed among these species, a remarkable gene rearrangement pattern of non-tandemly copied genes situated within tandemly-copied regions was commonly found. Furthermore, the existence of concerted evolution was observed between non-neighboring copies of triplicated 12S and 16S ribosomal RNA regions.ConclusionsPhylogenetic analyses based on mitogenomic data support a close relationship between Afrobatrachia and Microhylidae, with their estimated divergence 100 million years ago consistent with present-day endemism of afrobatrachians on the African continent. The afrobatrachian mt data supported the first tandem and second non-tandem duplication model for mt gene rearrangements and the recombination-based model for concerted evolution of duplicated mt regions. We also showed that specific nucleotide substitution and compositional patterns expected in duplicated and rearranged mt genes did not occur, suggesting no disadvantage in employing these genes for phylogenetic inference.
Highlights
Mitochondrial genomic reorganizations are rarely found in closely-related animals, yet drastic reorganizations have been found in the Ranoides frogs
Animal mitochondrial genomes typically consist of a closed circular molecule 16–17 kilo base pairs in size, with multiple copies existing in every cell [1]
We reviewed the phylogenetic relationships of afrobatrachians using the largest molecular dataset yet applied to this group
Summary
Mitochondrial genomic (mitogenomic) reorganizations are rarely found in closely-related animals, yet drastic reorganizations have been found in the Ranoides frogs. Most animal mt genomes contain the same 37 genes: 12S and 16S ribosomal RNA genes (12S and 16S rrns), 22 transfer RNA genes (trns), and 13 protein-coding genes (ATPase subunits 6 and 8: atp and 8; cytochrome oxidase subunits I, II and III: co; cytochrome b apoenzyme: cytb; and nicotinamide adenine dinucleotide dehydrogenase subunits 1–6 and 4 L: nd and 4 L) [2,3]. Of these 37 genes, 28 are encoded on the heavier guanine-rich DNA strand (H-strand), while nine are encoded on the cytosine-rich light strand (L-strand). 70% of molecular phylogenetic studies on animal taxa have used mt gene data [12]
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