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Abstract
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Biology
Evolutionary Biology

Phylogeny of Arthropoda Inferred From Mitochondrial Sequences: Strategies for Limiting the Misleading Effects of Multiple Changes In Pattern and Rates of Substitution

Profile image of Alexandre HassaninAlexandre Hassanin

2006, Molecular phylogenetics and evolution

https://doi.org/10.1016/J.YMPEV.2005.09.012Last updated
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17 pages

Abstract
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Arthropods, comprising a vast and diverse group of animals, present significant challenges in understanding their phylogenetic relationships. This study investigates mitochondrial DNA sequences across various arthropod lineages to clarify their evolutionary connections and proposes strategies to mitigate the misleading effects of multiple substitution events. The results emphasize the importance of genetic data in resolving contentious hypotheses surrounding arthropod phylogeny.

Key takeaways
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  1. Mitochondrial sequences reveal contentious relationships among the four subphyla of Arthropoda.
  2. The study utilizes a sample of 84 taxa, analyzing 6 specific mitochondrial protein-coding genes.
  3. Long-branch attraction (LBA) artifacts significantly affect phylogenetic inference from mtDNA sequences.
  4. The 'Neutral Transitions Excluded' (NTE) model improves phylogenetic signal by minimizing bias in data.
  5. Independent reversals of strand-bias complicate the interpretation of mitochondrial genome evolution.

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About the author
Alexandre Hassanin
Muséum National d'Histoire Naturelle, Faculty Member
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Related papers

Mitochondrial genome data alone are not enough to unambiguously resolve the relationships of Entognatha, Insecta and Crustacea sensu lato (Arthropoda)
Cyrille A . D'Haese

Cladistics, 2004

An analysis of the relationships of the major arthropod groups was undertaken using mitochondrial genome data to examine the hypotheses that Hexapoda is polyphyletic and that Collembola is more closely related to branchiopod crustaceans than insects. We sought to examine the sensitivity of this relationship to outgroup choice, data treatment, gene choice and optimality criteria used in the phylogenetic analysis of mitochondrial genome data. Additionally we sequenced the mitochondrial genome of an archaeognathan, Nesomachilis australica, to improve taxon selection in the apterygote insects, a group poorly represented in previous mitochondrial phylogenies. The sister group of the Collembola was rarely resolved in our analyses with a significant level of support. The use of different outgroups (myriapods, nematodes, or annelids + mollusks) resulted in many different placements of Collembola. The way in which the dataset was coded for analysis (DNA, DNA with the exclusion of third codon position and as amino acids) also had marked affects on tree topology. We found that nodal support was spread evenly throughout the 13 mitochondrial genes and the exclusion of genes resulted in significantly less resolution in the inferred trees. Optimality criteria had a much lesser effect on topology than the preceding factors; parsimony and Bayesian trees for a given data set and treatment were quite similar. We therefore conclude that the relationships of the extant arthropod groups as inferred by mitochondrial genomes are highly vulnerable to outgroup choice, data treatment and gene choice, and no consistent alternative hypothesis of Collembola's relationships is supported. Pending the resolution of these identified problems with the application of mitogenomic data to basal arthropod relationships, it is difficult to justify the rejection of hexapod monophyly, which is well supported on morphological grounds.

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Can comprehensive background knowledge be incorporated into substitution models to improve phylogenetic analyses? A case study on major arthropod relationships
Nikolaus U Szucsich, Heike Hadrys, Günther Pass

BMC Evolutionary Biology, 2009

Background: Whenever different data sets arrive at conflicting phylogenetic hypotheses, only testable causal explanations of sources of errors in at least one of the data sets allow us to critically choose among the conflicting hypotheses of relationships. The large (28S) and small (18S) subunit rRNAs are among the most popular markers for studies of deep phylogenies. However, some nodes supported by this data are suspected of being artifacts caused by peculiarities of the evolution of these molecules. Arthropod phylogeny is an especially controversial subject dotted with conflicting hypotheses which are dependent on data set and method of reconstruction. We assume that phylogenetic analyses based on these genes can be improved further i) by enlarging the taxon sample and ii) employing more realistic models of sequence evolution incorporating nonstationary substitution processes and iii) considering covariation and pairing of sites in rRNA-genes.

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Arthropod fossil data increase congruence of morphological and molecular phylogenies
David Legg

The interrelationships of major arthropod clades have long been contentious, but refinements in molecular phylogenetics underpin an emerging consensus. Striking topologies from these studies include the position of hexapods (insects) within a paraphyletic Crustacea, and a putative myriapod/chelicerate alliance. Although some morphological characters support these groupings, they have not been recovered in large-scale phylogenetic analyses based on morphology. An analysis herein of 753 morphological characters for 309 fossil and Recent panarthropods shows enhanced congruence with molecular phylogenies. We resolve hexapods within Crustacea, with remipedes their closest extant relatives. Selective taxon and character removal exposes the traditional myriapod/hexapod linkage as an artefact of convergent character acquisition during terrestrialisation. Fossils break up such long branches, their intermediate morphologies linking clades that have otherwise had their ancestral conditions overprinted. Pycnogonids are an exemplar, grouping with euchelicerates when fossils are included, and as sister-taxon to all other extant arthropods when fossils are removed.

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Arachnid Relationships Based on Mitochondrial Genomes: Asymmetric Nucleotide and Amino Acid Bias Affects Phylogenetic Analyses
Stuart Longhorn

Molecular Phylogenetics and …, 2009

Phylogenetic analyses based on mitochondrial DNA have yielded widely differing relationships among members of the arthropod lineage Arachnida, depending on the nucleotide coding schemes and models of evolution used. We enhanced taxonomic coverage within the Arachnida greatly by sequencing seven new arachnid mitochondrial genomes from five orders. We then used all 13 mitochondrial protein-coding genes from these genomes to evaluate patterns of nucleotide and amino acid biases. Our data show that two of the six orders of arachnids (spiders and scorpions) have experienced shifts in both nucleotide and amino acid usage in all their protein-coding genes, and that these biases mislead phylogeny reconstruction. These biases are most striking for the hydrophobic amino acids isoleucine and valine, which appear to have evolved asymmetrical exchanges in response to shifts in nucleotide composition. To improve phylogenetic accuracy based on amino acid differences, we tested two recoding methods: (1) removing all isoleucine and valine sites and (2) recoding amino acids based on their physiochemical properties. We find that these methods yield phylogenetic trees that are consistent in their support of ancient intraordinal divergences within the major arachnid lineages. Further refinement of amino acid recoding methods may help us better delineate interordinal relationships among these diverse organisms.

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First Molecular Evidence for the Existence of a Tardigrada + Arthropoda Clade
Gonzalo Giribet

The complete 18s rDNA gene sequence of Mucrobiotus group hufelundi (Tardigrada) was obtained and aligned with 18s rDNA and rRNA gene sequences of 24 metazoans (mainly protostomes). Discrete character (maximumparsimony) and distance (neighbor-joining) methods were used to infer their phylogeny. The evolution of bootstrap proportions with sequence length (pattern of resolved nodes, PRN) was studied to test the resolution of the nodes in neighbor-joining trees. The results show that arthropods are monophyletic. Tardigrades represent the sister group of arthropods (in parsimony analyses) or they are related with crustaceans (distance analysis and PRN). Arthropoda are divided into two main evolutionary lines, the Hexapoda + Crustacea line (weakly supported), and the Myriapoda + Chelicerata line. The Hexapoda + Crustacea line includes Pentastomida, but the internal resolution is far from clear. The Insecta (Ectognatha) are monophyletic, but no evidence for the monophyly of Hexapoda is found. The Chelicerata are a monophyletic group and the Myriapoda cluster close to Arachnida. Overall, the results obtained represent the first molecular evidence for a Tardigrada + Arthropoda clade. In addition, the congruence between molecular phylogenies of the Arthropoda from other authors and this obtained here indicates the need to review those obtained solely on morphological characters.

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    Molecular data on two mitochondrial genes of a newly discovered crustacean species ( Lightiella magdalenina, Cephalocarida)
    Paolo Francalacci

    Journal of The Marine Biological Association of The United Kingdom, 2010

    Cephalocarida is a rare and poorly known class of small benthic crustaceans, consisting of only eleven species belonging to five genera. Thus far, only one species (Hutchinsoniella macracantha) has been studied at molecular level. We report the partial sequences of two phylogenetically important mitochondrial genes (Cytochrome c Oxidase I and Cytochrome b) from the newly discovered Mediterranean species, Lightiella magdalenina. The genetic relationships between the two cephalocarid species are discussed.

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    The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida
    Lars Podsiadlowski

    BMC Genomics, 2006

    Background: Mitochondrial genomes form units of genetic information replicating indepentently from nuclear genomes. Sequence data (most often from protein-coding genes) and other features (gene order, RNA secondary structure) of mitochondrial genomes are often used in phylogenetic studies of metazoan animals from population to phylum level. Pycnogonids are primarily marine arthropods, often considered closely related to chelicerates (spiders, scorpions and allies). However, due to their aberrant morphology and to controversial results from molecular studies, their phylogenetic position is still under debate.

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    The complete mitochondrial genome of Pseudocellus pearsei (Chelicerata: Ricinulei) and a comparison of mitochondrial gene rearrangements in Arachnida
    Lars Podsiadlowski

    BMC Genomics, 2007

    Background: Mitochondrial genomes are widely utilized for phylogenetic and population genetic analyses among animals. In addition to sequence data the mitochondrial gene order and RNA secondary structure data are used in phylogenetic analyses. Arachnid phylogeny is still highly debated and there is a lack of sufficient sequence data for many taxa. Ricinulei (hooded tickspiders) are a morphologically distinct clade of arachnids with uncertain phylogenetic affinities.

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    The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features
    Lars Podsiadlowski

    BMC Genomics, 2006

    Background: Sequence data and other characters from mitochondrial genomes (gene translocations, secondary structure of RNA molecules) are useful in phylogenetic studies among metazoan animals from population to phylum level. Moreover, the comparison of complete mitochondrial sequences gives valuable information about the evolution of small genomes, e.g. about different mechanisms of gene translocation, gene duplication and gene loss, or concerning nucleotide frequency biases.

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    New Views on Strand Asymmetry in Insect Mitochondrial Genomes
    Cornelis van Achterberg

    PLOS One, 2010

    Strand asymmetry in nucleotide composition is a remarkable feature of animal mitochondrial genomes. Understanding the mutation processes that shape strand asymmetry is essential for comprehensive knowledge of genome evolution, demographical population history and accurate phylogenetic inference. Previous studies found that the relative contributions of different substitution types to strand asymmetry are associated with replication alone or both replication and transcription. However, the relative contributions of replication and transcription to strand asymmetry remain unclear.

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