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      Sequencing of the complete mitochondrial genome of a fish-parasitic flatworm Paratetraonchoides inermis (Platyhelminthes: Monogenea): tRNA gene arrangement reshuffling and implications for phylogeny

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          Paratetraonchoides inermis (Monogenea: Tetraonchoididae) is a flatworm parasitising the gills of uranoscopid fishes. Its morphological characteristics are ambiguous, and molecular data have never been used to study its phylogenetic relationships, which makes its taxonomic classification controversial. Also, several decades of unsuccessful attempts to resolve the relationships within the Monogenea present a strong indication that morphological datasets may not be robust enough to be used to infer evolutionary histories. As the use of molecular data is currently severely limited by their scarcity, we have sequenced and characterized the complete mitochondrial (mt) genome of P. inermis. To investigate its phylogenetic position, we performed phylogenetic analyses using Bayesian inference and maximum likelihood approaches using concatenated amino acid sequences of all 12 protein-coding genes on a dataset containing all available monogenean mt genomes.


          The circular mt genome of P. inermis (14,654 bp) contains the standard 36 genes: 22 tRNAs, two rRNAs, 12 protein-encoding genes (PCGs; Atp8 is missing) and a major non-coding region (mNCR). All genes are transcribed from the same strand. The A + T content of the whole genome (82.6%), as well as its elements, is the highest reported among the monogeneans thus far. Three tRNA-like cloverleaf structures were found in mNCR. Several results of the phylogenomic analysis are in disagreement with previously proposed relationships: instead of being closely related to the Gyrodactylidea, Tetraonchidea exhibit a phylogenetic affinity with the Dactylogyridea + Capsalidea clade; and the order Capsalidea is neither basal within the subclass Monopisthocotylea, nor groups with the Gyrodactylidea, but instead forms a sister clade with the Dactylogyridea. The mt genome of P. inermis exhibits a unique gene order, with an extensive reorganization of tRNAs. Monogenea exhibit exceptional gene order plasticity within the Neodermata.


          This study shows that gene order within monopisthocotylid mt genomes is evolving at uneven rates, which creates misleading evolutionary signals. Furthermore, our results indicate that all previous attempts to resolve the evolutionary history of the Monogenea may have produced at least partially erroneous relationships. This further corroborates the necessity to generate more molecular data for this group of parasitic animals.

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          The online version of this article (10.1186/s13071-017-2404-1) contains supplementary material, which is available to authorized users.

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          ProtTest: selection of best-fit models of protein evolution.

          Using an appropriate model of amino acid replacement is very important for the study of protein evolution and phylogenetic inference. We have built a tool for the selection of the best-fit model of evolution, among a set of candidate models, for a given protein sequence alignment. ProtTest is available under the GNU license from http://darwin.uvigo.es
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            Rare genomic changes as a tool for phylogenetics.

            DNA sequence data have offered valuable insights into the relationships between living organisms. However, most phylogenetic analyses of DNA sequences rely primarily on single nucleotide substitutions, which might not be perfect phylogenetic markers. Rare genomic changes (RGCs), such as intron indels, retroposon integrations, signature sequences, mitochondrial and chloroplast gene order changes, gene duplications and genetic code changes, provide a suite of complementary markers with enormous potential for molecular systematics. Recent exploitation of RGCs has already started to yield exciting phylogenetic information.
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              The Diversity of Parasites


                Author and article information

                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                10 October 2017
                10 October 2017
                : 10
                [1 ]ISNI 0000 0004 1792 6029, GRID grid.429211.d, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, , Institute of Hydrobiology, Chinese Academy of Sciences, ; Wuhan, People’s Republic of China
                [2 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, University of Chinese Academy of Sciences, ; Beijing, People’s Republic of China
                [3 ]Bio-Transduction Lab, Wuhan Institute of Biotechnology, Wuhan, People’s Republic of China
                © The Author(s). 2017

                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.

                Funded by: The Earmarked Fund for China Agriculture Research System
                Award ID: CARS-45-15
                Award Recipient :
                Funded by: The National Natural Science Foundation of China
                Award ID: 31572658
                Award Recipient :
                Funded by: The Major Scientific and Technological Innovation Project of Hubei Province
                Award ID: 2015ABA045
                Award Recipient :
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