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      Fragmented mitochondrial genomes in two suborders of parasitic lice of eutherian mammals (Anoplura and Rhynchophthirina, Insecta)

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          Abstract

          Parasitic lice (order Phthiraptera) infest birds and mammals. The typical animal mitochondrial (mt) genome organization, which consists of a single chromosome with 37 genes, was found in chewing lice in the suborders Amblycera and Ischnocera. The sucking lice (suborder Anoplura) known, however, have fragmented mt genomes with 9–20 minichromosomes. We sequenced the mt genome of the elephant louse, Haematomyzus elephantis – the first species of chewing lice investigated from the suborder Rhynchophthirina. We identified 33 mt genes in the elephant louse, which were on 10 minichromosomes. Each minichromosome is 3.5–4.2 kb in size and has 2–6 genes. Phylogenetic analyses of mt genome sequences confirm that the elephant louse is more closely related to sucking lice than to the chewing lice in the Amblycera and Ischnocera. Our results indicate that mt genome fragmentation is shared by the suborders Anoplura and Rhynchophthirina. Nine of the 10 mt minichromosomes of the elephant louse differ from those of the sucking lice (Anoplura) known in gene content and gene arrangement, indicating that distinct mt karyotypes have evolved in Anoplura and Rhynchophthirina since they diverged ~92 million years ago.

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          The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus.

          The mitochondrial (mt) genomes of animals typically consist of a single circular chromosome that is approximately 16-kb long and has 37 genes. Our analyses of the sequence reads from the Human Body Louse Genome Project and the patterns of gel electrophoresis and Southern hybridization revealed a novel type of mt genome in the sucking louse, Pediculus humanus. Instead of having all mt genes on a single chromosome, the 37 mt genes of this louse are on 18 minicircular chromosomes. Each minicircular chromosome is 3-4 kb long and has one to three genes. Minicircular mt chromosomes are also present in the four other species of sucking lice that we investigated, but not in chewing lice nor in the Psocoptera, to which sucking lice are most closely related. We also report unequivocal evidence for recombination between minicircular mt chromosomes in P. humanus and for sequence variation in mt genes generated by recombination. The advantages of a fragmented mt genome, if any, are currently unknown. Fragmentation of mt genome, however, has coevolved with blood feeding in the sucking lice. It will be of interest to explore whether or not life history features are associated with the evolution of fragmented chromosomes.
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            Key transitions in animal evolution: a mitochondrial DNA perspective.

            Animal mitochondrial DNA (mtDNA) is usually depicted as a small and very economically organized molecule with almost invariable gene content, stable gene order, a high rate of sequence evolution, and several unorthodox genetic features. Sampling across different animal phyla reveals that such a description applies primarily to mtDNA of bilaterian animals (such as arthropods or chordates). By contrast, mitochondrial genomes of nonbilaterian animals (phyla Cnidaria, Placozoa, and Porifera) display more variation in size and gene content and, in most cases, lack the genetic novelties associated with bilaterian mtDNA. Outside the Metazoa, mtDNA of the choanoflagellate Monosiga brevicollis, the closest unicellular out-group, is a much larger molecule that contains a large proportion of noncoding DNA, 1.5 times more genes, as well as several introns. Thus, changes in animal mtDNA organization appear to correlate with two main transitions in animal evolution: the origin of multicellularity and the origin of the Bilateria. Studies of mtDNA in nonbilaterian animals provide valuable insights into these transitions in the organization of mtDNA and also supply data for phylogenetic analyses of the relationships of early animals. Here I review recent progress in the understanding of nonbilaterian mtDNA and discuss the advantages and limitations of mitochondrial data sets for inferences about the phylogeny and evolution of animals.
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              Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects.

              A number of studies indicated that lineages of animals with high rates of mitochondrial (mt) gene rearrangement might have high rates of mt nucleotide substitution. We chose the hemipteroid assemblage and the Insecta to test the idea that rates of mt gene rearrangement and mt nucleotide substitution are correlated. For this purpose, we sequenced the mt genome of a lepidopsocid from the Psocoptera, the only order of hemipteroid insects for which an entire mtDNA sequence is not available. The mt genome of this lepidopsocid is circular, 16,924 bp long, and contains 37 genes and a putative control region; seven tRNA genes and a protein-coding gene in this genome have changed positions relative to the ancestral arrangement of mt genes of insects. We then compared the relative rates of nucleotide substitution among species from each of the four orders of hemipteroid insects and among the 20 insects whose mt genomes have been sequenced entirely. All comparisons among the hemipteroid insects showed that species with higher rates of gene rearrangement also had significantly higher rates of nucleotide substitution statistically than did species with lower rates of gene rearrangement. In comparisons among the 20 insects, where the mt genomes of the two species differed by more than five breakpoints, the more rearranged species always had a significantly higher rate of nucleotide substitution than the less rearranged species. However, in comparisons where the mt genomes of two species differed by five or less breakpoints, the more rearranged species did not always have a significantly higher rate of nucleotide substitution than the less rearranged species. We tested the statistical significance of the correlation between the rates of mt gene rearrangement and mt nucleotide substitution with nine pairs of insects that were phylogenetically independent from one another. We found that the correlation was positive and statistically significant (R2 = 0.73, P = 0.01; Rs = 0.67, P < 0.05). We propose that increased rates of nucleotide substitution may lead to increased rates of gene rearrangement in the mt genomes of insects.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                30 November 2015
                2015
                : 5
                : 17389
                Affiliations
                [1 ]GeneCology Research Centre, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast , Maroochydore, Queensland 4556, Australia
                [2 ]Parasitology Section, School of Chemistry and Molecular Biosciences, The University of Queensland , Queensland 4072, Australia
                [3 ]Department of Entomology, China. Agricultural University , Beijing 100193, China
                [4 ]Manitoba Health , Winnipeg, Manitoba, R2W 3C7, Canada
                Author notes
                Article
                srep17389
                10.1038/srep17389
                4663631
                26617060
                4011b083-ba10-4ce4-800d-c82892e6cb76
                Copyright © 2015, Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 21 August 2014
                : 29 October 2015
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