Abstract

The mitochondrial (mt) genome of the bushveld rain frog (Breviceps adspersus, Brevicipitidae, Afrobatrachia) is the largest (28.8 kbp) among the vertebrates investigated to date. The major cause of genome size enlargement in this species is the duplication of multiple genomic regions. To investigate the evolutionary lineage, timing, and process of mt genome enlargement, we sequenced the complete mtDNAs of two congeneric rain frogs, B. mossambicus and B. poweri. The mt genomic organization, gene content, and gene arrangements of these two rain frogs are very similar to each other but differ from those of B. adspersus. The B. mossambicus mt genome (22.5 kbp) does not differ significantly from that of most other afrobatrachians. In contrast, the B. poweri mtDNA (28.1 kbp) is considerably larger: currently the second largest among vertebrates, after B. adspersus. The main causes of genome enlargement differ among Breviceps species. Unusual elongation (12.5 kbp) of the control region (CR), a single major noncoding region of the vertebrate mt genome, is responsible for the extremely large mt genome in B. poweri. Based on the current Breviceps phylogeny and estimated divergence age, it can be concluded that the genome enlargements occurred independently in each species lineage within relatively short periods. Furthermore, a high nucleotide substitution rate and relaxation of selective pressures, which are considered to be involved in changes in genome size, were also detected in afrobatrachian lineages. Our results suggest that these factors were not direct causes but may have indirectly affected mt genome enlargements in Breviceps.

Highlights

  • Mitochondrial genomes of multicellular animals are generally closed-circular and double-stranded DNA molecules approximately 14–20 kbp in length [1,2,3]

  • Our results indicate that the huge mt genomes arose in two independent rain frog lineages within relatively short periods (>47 and >30 million years for the lineages leading to B. poweri and B. adspersus, respectively)

  • This study shows that the mt genomes of B. poweri and B. mossambicus are not markedly rearranged from the typical neobatrachian type, B. adspersus branches between these species’ lineages (Figure 1 and see [54])

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Summary

Introduction

Mitochondrial (mt) genomes of multicellular animals (metazoans) are generally closed-circular and double-stranded DNA molecules approximately 14–20 kbp in length [1,2,3]. Genome size ranges from 6 to 48 kbp [2, 4], and linear and fragmented mtDNAs have been found in approximately 9000 animals investigated far [5,6,7]. In most metazoans, this small organelle genome encodes a typical set of 37 genes: 13 protein genes, involved in the electron transport system of respiration, two rRNA genes (rrns), and 22 tRNA genes (trns). Hoplobatrachus tigerinus 20.5 kbp Fejervarya limnonectes 17.7 kbp Limnonectes fujianensis 18.3 kbp Sooglossus sechellensis NA

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