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      Mitochondrial Genome Fragmentation Unites the Parasitic Lice of Eutherian Mammals

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          Abstract

          Organelle genome fragmentation has been found in a wide range of eukaryotic lineages; however, its use in phylogenetic reconstruction has not been demonstrated. We explored the use of mitochondrial (mt) genome fragmentation in resolving the controversial suborder-level phylogeny of parasitic lice (order Phthiraptera). There are approximately 5000 species of parasitic lice in four suborders (Amblycera, Ischnocera, Rhynchophthirina, and Anoplura), which infest mammals and birds. The phylogenetic relationships among these suborders are unresolved despite decades of studies. We sequenced the mt genomes of eight species of parasitic lice and compared them with 17 other species of parasitic lice sequenced previously. We found that the typical single-chromosome mt genome is retained in the lice of birds but fragmented into many minichromosomes in the lice of eutherian mammals. The shared derived feature of mt genome fragmentation unites the eutherian mammal lice of Ischnocera (family Trichodectidae) with Anoplura and Rhynchophthirina to the exclusion of the bird lice of Ischnocera (family Philopteridae). The novel clade, namely Mitodivisia, is also supported by phylogenetic analysis of mt genome and cox1 gene sequences. Our results demonstrate, for the first time, that organelle genome fragmentation is informative for resolving controversial high-level phylogenies.

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          Most cited references49

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          TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

          We present TranslatorX, a web server designed to align protein-coding nucleotide sequences based on their corresponding amino acid translations. Many comparisons between biological sequences (nucleic acids and proteins) involve the construction of multiple alignments. Alignments represent a statement regarding the homology between individual nucleotides or amino acids within homologous genes. As protein-coding DNA sequences evolve as triplets of nucleotides (codons) and it is known that sequence similarity degrades more rapidly at the DNA than at the amino acid level, alignments are generally more accurate when based on amino acids than on their corresponding nucleotides. TranslatorX novelties include: (i) use of all documented genetic codes and the possibility of assigning different genetic codes for each sequence; (ii) a battery of different multiple alignment programs; (iii) translation of ambiguous codons when possible; (iv) an innovative criterion to clean nucleotide alignments with GBlocks based on protein information; and (v) a rich output, including Jalview-powered graphical visualization of the alignments, codon-based alignments coloured according to the corresponding amino acids, measures of compositional bias and first, second and third codon position specific alignments. The TranslatorX server is freely available at http://translatorx.co.uk.
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            Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species.

            The mitochondrial genome (mtDNA) of Metazoa is a good model system for evolutionary genomic studies and the availability of more than 1000 sequences provides an almost unique opportunity to decode the mechanisms of genome evolution over a large phylogenetic range. In this paper, we review several structural features of the metazoan mtDNA, such as gene content, genome size, genome architecture and the new parameter of gene strand asymmetry in a phylogenetic framework. The data reviewed here show that: (1) the plasticity of Metazoa mtDNA is higher than previously thought and mainly due to variation in number and location of tRNA genes; (2) an exceptional trend towards stabilization of genomic features occurred in deuterostomes and was exacerbated in vertebrates, where gene content, genome architecture and gene strand asymmetry are almost invariant. Only tunicates exhibit a very high degree of genome variability comparable to that found outside deuterostomes. In order to analyse the genomic evolutionary process at short evolutionary distances, we have also compared mtDNAs of species belonging to the same genus: the variability observed in congeneric species significantly recapitulates the evolutionary dynamics observed at higher taxonomic ranks, especially for taxa showing high levels of genome plasticity and/or fast nucleotide substitution rates. Thus, the analysis of congeneric species promises to be a valuable approach for the assessment of the mtDNA evolutionary trend in poorly or not yet sampled metazoan groups.
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              Big trees from little genomes: mitochondrial gene order as a phylogenetic tool.

              Gene arrangement comparisons are a powerful tool for phylogenetic studies, especially those focused on ancient relationships. Recent reports using metazoan mitochondrial genomes address evolutionary relationships as well as rates and mechanisms of rearrangement. Mitochondrial systems serve as a model for larger-scale comparisons of whole organismal genomes and a stimulus for developing methods for reconstructing the patterns of rearrangement.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Syst Biol
                Syst. Biol
                sysbio
                Systematic Biology
                Oxford University Press
                1063-5157
                1076-836X
                May 2019
                17 September 2018
                17 September 2018
                : 68
                : 3
                : 430-440
                Affiliations
                [1 ]Key Laboratory of Pest Monitoring and Green Management, Ministry of Agriculture, Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
                [2 ]Hunan Provincial Key Laboratory of Protein Engineering in Animal Vaccines, College of Veterinary Medicine, Hunan Agricultural University, Changsha, Hunan Province 410128, China
                [3 ]School of Science and Engineering, GeneCology Research Centre, Animal Research Centre, University of the Sunshine Coast, Sippy Downs, Queensland 4556, Australia
                [4 ]Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Dutton Park, Queensland, Australia
                [5 ]Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada
                Author notes
                Correspondence to be sent to: School of Science and Engineering, GeneCology Research Centre, Animal Research Centre, University of the Sunshine Coast, Sippy Downs, Queensland 4556, Australia; E-mail: rshao@ 123456usc.edu.au .
                Article
                syy062
                10.1093/sysbio/syy062
                6472445
                30239978
                73cb7af3-e0ec-4b61-ba77-8d03088f2ca4
                © The Author(s) 2018. Published by Oxford University Press, on behalf of the Society of Systematic Biologists.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contactjournals.permissions@ 123456oup.com

                History
                : 28 March 2018
                : 11 September 2018
                : 12 September 2018
                Page count
                Pages: 11
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31420103902
                Award ID: 31730086
                Funded by: Beijing Natural Science Foundation 10.13039/501100004826
                Award ID: 6152016
                Award ID: 6144027
                Funded by: China Postdoctoral Science Foundation 10.13039/501100002858
                Award ID: 2016M601178
                Funded by: Training Program for Excellent Young Innovators of Changsha
                Award ID: KQ1707005
                Funded by: Australia-China Science and Research Fund Group Mission
                Award ID: ACSRF00980
                Funded by: Australian Research Council 10.13039/501100000923
                Award ID: DP120100240
                Categories
                Regular Articles

                Animal science & Zoology
                genome fragmentation,mitochondrial genome,parasitic lice,phylogeny
                Animal science & Zoology
                genome fragmentation, mitochondrial genome, parasitic lice, phylogeny

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