Abstract

BackgroundThe animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation. As more mitochondrial genomes are sequenced, mitochondrial duplications and gene rearrangements have been frequently identified among diverse animal groups. Although several mechanisms of gene rearrangement have been proposed thus far, more observational evidence from major taxa is needed to validate specific mechanisms. In the current study, the complete mitochondrial DNA of sixteen bird species from the family Ardeidae was sequenced and the evolution of mitochondrial gene rearrangements was investigated. The mitochondrial genomes were then used to review the phylogenies of these ardeid birds.ResultsThe complete mitochondrial genome sequences of the sixteen ardeid birds exhibited four distinct mitochondrial gene orders in which two of them, named as “duplicate tRNAGlu–CR” and “duplicate tRNAThr–tRNAPro and CR”, were newly discovered. These gene rearrangements arose from an evolutionary process consistent with the tandem duplication - random loss model (TDRL). Additionally, duplications in these gene orders were near identical in nucleotide sequences within each individual, suggesting that they evolved in concert. Phylogenetic analyses of the sixteen ardeid species supported the idea that Ardea ibis, Ardea modesta and Ardea intermedia should be classified as genus Ardea, and Ixobrychus flavicollis as genus Ixobrychus, and indicated that within the subfamily Ardeinae, Nycticorax nycticorax is closely related to genus Egretta and that Ardeola bacchus and Butorides striatus are closely related to the genus Ardea.ConclusionsThe duplicate tRNAThr–CR gene order is found in most ardeid lineages, suggesting this gene order is the ancestral pattern within these birds and persisted in most lineages via concerted evolution. In two independent lineages, when the concerted evolution stopped in some subsections due to the accumulation of numerous substitutions and deletions, the duplicate tRNAThr–CR gene order was transformed into three other gene orders. The phylogenetic trees produced from concatenated rRNA and protein coding genes have high support values in most nodes, indicating that the mitochondrial genome sequences are promising markers for resolving the phylogenetic issues of ardeid birds when more taxa are added.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-573) contains supplementary material, which is available to authorized users.

Highlights

  • The animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation

  • There are differences among the various copies and arrangements of the control region (CR) and flanking genes among these five mt gene orders, which were assumed to have resulted from the evolutionary process, tandem duplication and random loss (TDRL)

  • Gene content and order of CR and flanking genes In this study, the complete mitochondrial DNA sequences were obtained for sixteen ardeid birds, which had been deposited in NCBI GenBank under accession numbers KJ190944 to KJ190959

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Summary

Introduction

The animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation. Gibb et al [8] introduced a naming system of avian mt gene orders according to these variations, known as ancestral avian, remnant CR (2), duplicate CR and duplicate tRNAThr– CR. These were initially identified in the chicken [1], falcon [2], Amazona parrot [5] and albatross [7]. In ancestral avian gene order, the gene content and arrangement in the region located between cytochrome b (Cytb) and tRNAPhe is Cytb, tRNAThr, tRNAPro, ND6, tRNAGlu and CR These genes and the CR are tandem duplicated in the duplicate tRNAThr–CR gene order, but the second Cytb is only a partial copy (p-Cytb). Verkuil et al [13] identified a novel mt gene order in the ruff, which differs from the duplicate tRNAThr–CR gene order in the degeneration of the second tRNAThr

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