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      Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri

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          Abstract

          Background

          Tandem duplication followed by random loss (TDRL) is the most frequently invoked model to explain the diversity of gene rearrangements in metazoan mitogenomes. The initial stages of gene rearrangement are difficult to observe in nature, which limits our understanding of incipient duplication events and the subsequent process of random loss. Intraspecific gene reorganizations may represent intermediate states, and if so they potentially shed light on the evolutionary dynamics of TDRL.

          Results

          Nucleotide sequences in a hotspot of gene-rearrangement in 28 populations of a single species of frog, Quasipaa boulengeri, provide such predicted intermediate states. Gene order and phylogenetic analyses support a single tandem duplication event and a step-by-step process of random loss. Intraspecific gene rearrangements are not commonly found through comparison of all mitochondrial DNA records of amphibians and squamate reptiles in GenBank.

          Conclusions

          The intraspecific variation in Q. boulengeri provides insights into the rate of partial duplications and deletions within a mitogenome, and reveals that fixation and gene-distribution in mitogenomic reorganization is likely non-adaptive.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12864-016-3309-7) contains supplementary material, which is available to authorized users.

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          Most cited references38

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          Mutation pressure and the evolution of organelle genomic architecture.

          The nuclear genomes of multicellular animals and plants contain large amounts of noncoding DNA, the disadvantages of which can be too weak to be effectively countered by selection in lineages with reduced effective population sizes. In contrast, the organelle genomes of these two lineages evolved to opposite ends of the spectrum of genomic complexity, despite similar effective population sizes. This pattern and other puzzling aspects of organelle evolution appear to be consequences of differences in organelle mutation rates. These observations provide support for the hypothesis that the fundamental features of genome evolution are largely defined by the relative power of two nonadaptive forces: random genetic drift and mutation pressure.
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            Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia.

            Asian frogs of the tribe Paini (Anura: Dicroglossidae) range across several first-order tectono-morphological domains of the Cenozoic Indo-Asian collision that include the Tibetan Plateau, the Himalayas, and Indochina. We show how the tectonic events induced by the Indo-Asian collision affected the regional biota and, in turn, how the geological history of the earth can be viewed from a biological perspective. Our analysis of a concatenated dataset comprising four nuclear gene sequences of Paini revealed two main radiations, corresponding to the genera Nanorana (I) and Quasipaa (II). Five distinct clades are recognized: Tibetan plateau clade (I-1), Himalaya clade (I-2), environs of Himalaya-Tibetan plateau clade (I-3), South China clade (II-1), and Indochina clade (II-2). This pattern of relationships highlights the significance of geography in shaping evolutionary history. Building on our molecular dating, ancestral region reconstruction, and distributional patterns, we hypothesize a distinct geographic and climatic transition in Asia beginning in the Oligocene and intensifying in the Miocene; this stimulated rapid diversification of Paini. Vicariance explains species formation among major lineages within Nanorana. Dispersal, in contrast, plays an important role among Quasipaa, with the southern Chinese taxa originating from Indochina. Our results support the tectonic hypothesis that an uplift in the Himalaya-Tibetan plateau region resulting from crustal thickening and lateral extrusion of Indochina occurred synchronously during the transition between Oligocene and Miocene in reaction to the Indo-Asian collision. The phylogenetic history of Paini illuminates critical aspects of the timing of geological events responsible for the current geography of Southeast Asia.
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              The use of genome-level characters for phylogenetic reconstruction.

              Now that large-scale genome-sequencing projects are sampling many organismal lineages, it is becoming possible to compare large data sets of not only DNA and protein sequences, but also genome-level features, such as gene arrangements and the positions of mobile genetic elements. Although it is unlikely that comparisons of such features will address a large number of evolutionary branch points across the broad tree of life owing to the infeasibility of such sampling, they have great potential for resolving many crucial, contested relationships for which no other data seem promising. Here, I discuss the advancements, advantages, methods, and problems of the use of genome-level characters for reconstructing evolutionary relationships.
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                Author and article information

                Contributors
                xiayun@cib.ac.cn
                zhengyc@cib.ac.cn
                bob.murphy.ca@gmail.com
                zengxm@cib.ac.cn
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                24 November 2016
                24 November 2016
                2016
                : 17
                : 965
                Affiliations
                [1 ]Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041 China
                [2 ]Centre for Biodiversity, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6 Canada
                Article
                3309
                10.1186/s12864-016-3309-7
                5122201
                27881087
                57355b8d-2ba7-4ae9-82e8-5d8723cf5ef1
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 19 July 2016
                : 17 November 2016
                Funding
                Funded by: National Natural Sciences Foundation of China
                Award ID: 31372181
                Award ID: 31401960
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31572243
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Genetics
                mitochondrial gene order,trna,mitogenomics,intermediate mitogenomic rearrangement,random gene loss

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