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Comparative analysis of mitochondrial genomes in Diplura (hexapoda, arthropoda): taxon sampling is crucial for phylogenetic inferences.

ABSTRACT: Two-pronged bristletails (Diplura) are traditionally classified into three major superfamilies: Campodeoidea, Projapygoidea, and Japygoidea. The interrelationships of these three superfamilies and the monophyly of Diplura have been much debated. Few previous studies included Projapygoidea in their phylogenetic considerations, and its position within Diplura still is a puzzle from both morphological and molecular points of view. Until now, no mitochondrial genome has been sequenced for any projapygoid species. To fill in this gap, we determined and annotated the complete mitochondrial genome of Octostigma sinensis (Octostigmatidae, Projapygoidea), and of three more dipluran species, one each from the Campodeidae, Parajapygidae, and Japygidae. All four newly sequenced dipluran mtDNAs encode the same set of genes in the same gene order as shared by most crustaceans and hexapods. Secondary structure truncations have occurred in trnR, trnC, trnS1, and trnS2, and the reduction of transfer RNA D-arms was found to be taxonomically correlated, with Campodeoidea having experienced the most reduction. Partitioned phylogenetic analyses, based on both amino acids and nucleotides of the protein-coding genes plus the ribosomal RNA genes, retrieve significant support for a monophyletic Diplura within Pancrustacea, with Projapygoidea more closely related to Campodeoidea than to Japygoidea. Another key finding is that monophyly of Diplura cannot be recovered unless Projapygoidea is included in the phylogenetic analyses; this explains the dipluran polyphyly found by past mitogenomic studies. Including Projapygoidea increased the sampling density within Diplura and probably helped by breaking up a long-branch-attraction artifact. This finding provides an example of how proper sampling is significant for phylogenetic inference.

SUBMITTER: Chen WJ

PROVIDER: S-EPMC3914688 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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Comparative analysis of mitochondrial genomes in Diplura (hexapoda, arthropoda): taxon sampling is crucial for phylogenetic inferences.

Chen Wan-Jun WJ Koch Markus M Mallatt Jon M JM Luan Yun-Xia YX

Genome biology and evolution 20140101 1

Two-pronged bristletails (Diplura) are traditionally classified into three major superfamilies: Campodeoidea, Projapygoidea, and Japygoidea. The interrelationships of these three superfamilies and the monophyly of Diplura have been much debated. Few previous studies included Projapygoidea in their phylogenetic considerations, and its position within Diplura still is a puzzle from both morphological and molecular points of view. Until now, no mitochondrial genome has been sequenced for any projap ...[more]

PMID: 24391151

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Project description:BackgroundSnake mitochondrial genomes are of great interest in understanding mitogenomic evolution because of gene duplications and rearrangements and the fast evolutionary rate of their genes compared to other vertebrates. Mitochondrial gene sequences have also played an important role in attempts to resolve the contentious phylogenetic relationships of especially the early divergences among alethinophidian snakes. Two recent innovative studies found dramatic gene- and branch-specific relative acceleration in snake protein-coding gene evolution, particularly along internal branches leading to Serpentes and Alethinophidia. It has been hypothesized that some of these rate shifts are temporally (and possibly causally) associated with control region duplication and/or major changes in ecology and anatomy.ResultsThe near-complete mitochondrial (mt) genomes of three henophidian snakes were sequenced: Anilius scytale, Rhinophis philippinus, and Charina trivirgata. All three genomes share a duplicated control region and translocated tRNALEU, derived features found in all alethinophidian snakes studied to date. The new sequence data were aligned with mt genome data for 21 other species of snakes and used in phylogenetic analyses. Phylogenetic results agreed with many other studies in recovering several robust clades, including Colubroidea, Caenophidia, and Cylindrophiidae+Uropeltidae. Nodes within Henophidia that have been difficult to resolve robustly in previous analyses remained uncompellingly resolved here. Comparisons of relative rates of evolution of rRNA vs. protein-coding genes were conducted by estimating branch lengths across the tree. Our expanded sampling revealed dramatic acceleration along the branch leading to Typhlopidae, particularly long rRNA terminal branches within Scolecophidia, and that most of the dramatic acceleration in protein-coding gene rate along Serpentes and Alethinophidia branches occurred before Anilius diverged from other alethinophidians.ConclusionsMitochondrial gene sequence data alone may not be able to robustly resolve basal divergences among alethinophidian snakes. Taxon sampling plays an important role in identifying mitogenomic evolutionary events within snakes, and in testing hypotheses explaining their origin. Dramatic rate shifts in mitogenomic evolution occur within Scolecophidia as well as Alethinophidia, thus falsifying the hypothesis that these shifts in snakes are associated exclusively with evolution of a non-burrowing lifestyle, macrostomatan feeding ecology and/or duplication of the control region, both restricted to alethinophidians among living snakes.

Project description:BackgroundThe phylogenetic position of the Protura, traditionally considered the most basal hexapod group, is disputed because it has many unique morphological characters compared with other hexapods. Although mitochondrial genome information has been used extensively in phylogenetic studies, such information is not available for the Protura. This has impeded phylogenetic studies on this taxon, as well as the evolution of the arthropod mitochondrial genome.ResultsIn this study, the mitochondrial genome of Sinentomon erythranum was sequenced, as the first proturan species to be reported. The genome contains a number of special features that differ from those of other hexapods and arthropods. As a very small arthropod mitochondrial genome, its 14,491 nucleotides encode 37 typical mitochondrial genes. Compared with other metazoan mtDNA, it has the most biased nucleotide composition with T = 52.4%, an extreme and reversed AT-skew of -0.351 and a GC-skew of 0.350. Two tandemly repeated regions occur in the A+T-rich region, and both could form stable stem-loop structures. Eighteen of the 22 tRNAs are greatly reduced in size with truncated secondary structures. The gene order is novel among available arthropod mitochondrial genomes. Rearrangements have involved in not only small tRNA genes, but also PCGs (protein-coding genes) and ribosome RNA genes. A large block of genes has experienced inversion and another nearby block has been reshuffled, which can be explained by the tandem duplication and random loss model. The most remarkable finding is that trnL2(UUR) is not located between cox1 and cox2 as observed in most hexapod and crustacean groups, but is between rrnL and nad1 as in the ancestral arthropod ground pattern. The "cox1-cox2" pattern was further confirmed in three more representative proturan species. The phylogenetic analyses based on the amino acid sequences of 13 mitochondrial PCGs suggest S. erythranum failed to group with other hexapod groups.ConclusionsThe mitochondrial genome of S. erythranum shows many different features from other hexapod and arthropod mitochondrial genomes. It underwent highly divergent evolution. The "cox1-cox2" pattern probably represents the ancestral state for all proturan mitogenomes, and suggests a long evolutionary history for the Protura.

Dataset Information

Comparative analysis of mitochondrial genomes in Diplura (hexapoda, arthropoda): taxon sampling is crucial for phylogenetic inferences.

Publications

Comparative analysis of mitochondrial genomes in Diplura (hexapoda, arthropoda): taxon sampling is crucial for phylogenetic inferences.

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