Ecdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda

Omar Rota-Stabelli, Ehsan Kayal, Dianne Gleeson, Jennifer Daub, Jeffrey Boore, Maximilian Telford, Davide Pisani, Mark Blaxter, Dennis Lavrov

    Research output: Contribution to journalArticle

    110 Citations (Scopus)

    Abstract

    Ecdysozoa is the recently recognized clade of molting animals that comprises the vast majority of extant animal species and the most important invertebrate model organisms—the fruit fly and the nematode worm. Evolutionary relationships within the ecdysozoans remain, however, unresolved, impairing the correct interpretation of comparative genomic studies. In particular, the affinities of the three Panarthropoda phyla (Arthropoda, nychophora, and Tardigrada) and the position of Myriapoda within Arthropoda (Mandibulata vs. Myriochelata hypothesis) are among the most contentious issues in animal phylogenetics. To elucidate these relationships, we have determined and analyzed complete or nearly complete mitochondrial genome sequences of two Tardigrada, Hypsibius dujardini and Thulinia sp. (the first genomes to date for this phylum); one Priapulida, Halicryptus spinulosus; and two Onychophora, Peripatoides sp. and Epiperipatus biolleyi; and a partial mitochondrial genome sequence of the Onychophora Euperipatoides kanagrensis. Tardigrada mitochondrial genomes resemble those of the arthropods in term of the gene order and strand asymmetry, whereas Onychophora genomes are characterized by numerous gene order rearrangements and strand asymmetry variations. In addition, Onychophora genomes are extremely enriched in A and T nucleotides, whereas Priapulida and Tardigrada are more balanced. Phylogenetic analyses based on concatenated amino acid coding sequences support a monophyletic origin of the Ecdysozoa and the position of Priapulida as the sister group of a monophyletic Panarthropoda (Tardigrada plus Onychophora plus Arthropoda). The position of Tardigrada is more problematic, most likely because of long branch attraction (LBA). However, experiments designed to reduce LBA suggest that the most likely placement of Tardigrada is as a sister group of Onychophora. The same analyses also recover monophyly of traditionally recognized arthropod lineages such as Arachnida and of the highly debated clade Mandibulata.
    Original languageEnglish
    Pages (from-to)425-440
    Number of pages16
    JournalGenome Biology and Evolution
    Volume2
    DOIs
    Publication statusPublished - 2010

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    Tardigrada
    Onychophora
    Invertebrates
    Arthropods
    genome
    invertebrate
    invertebrates
    Arthropoda
    Mitochondrial Genome
    Gene Order
    arthropod
    Genome
    asymmetry
    Euperipatoides
    arthropods
    phylogenetics
    Arachnida
    Myriapoda
    gene
    animal

    Cite this

    Rota-Stabelli, Omar ; Kayal, Ehsan ; Gleeson, Dianne ; Daub, Jennifer ; Boore, Jeffrey ; Telford, Maximilian ; Pisani, Davide ; Blaxter, Mark ; Lavrov, Dennis. / Ecdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda. In: Genome Biology and Evolution. 2010 ; Vol. 2. pp. 425-440.
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    Rota-Stabelli, O, Kayal, E, Gleeson, D, Daub, J, Boore, J, Telford, M, Pisani, D, Blaxter, M & Lavrov, D 2010, 'Ecdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda', Genome Biology and Evolution, vol. 2, pp. 425-440. https://doi.org/10.1093/gbe/evq030

    Ecdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda. / Rota-Stabelli, Omar; Kayal, Ehsan; Gleeson, Dianne; Daub, Jennifer; Boore, Jeffrey; Telford, Maximilian; Pisani, Davide; Blaxter, Mark; Lavrov, Dennis.

    In: Genome Biology and Evolution, Vol. 2, 2010, p. 425-440.

    Research output: Contribution to journalArticle

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    T1 - Ecdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda

    AU - Rota-Stabelli, Omar

    AU - Kayal, Ehsan

    AU - Gleeson, Dianne

    AU - Daub, Jennifer

    AU - Boore, Jeffrey

    AU - Telford, Maximilian

    AU - Pisani, Davide

    AU - Blaxter, Mark

    AU - Lavrov, Dennis

    PY - 2010

    Y1 - 2010

    N2 - Ecdysozoa is the recently recognized clade of molting animals that comprises the vast majority of extant animal species and the most important invertebrate model organisms—the fruit fly and the nematode worm. Evolutionary relationships within the ecdysozoans remain, however, unresolved, impairing the correct interpretation of comparative genomic studies. In particular, the affinities of the three Panarthropoda phyla (Arthropoda, nychophora, and Tardigrada) and the position of Myriapoda within Arthropoda (Mandibulata vs. Myriochelata hypothesis) are among the most contentious issues in animal phylogenetics. To elucidate these relationships, we have determined and analyzed complete or nearly complete mitochondrial genome sequences of two Tardigrada, Hypsibius dujardini and Thulinia sp. (the first genomes to date for this phylum); one Priapulida, Halicryptus spinulosus; and two Onychophora, Peripatoides sp. and Epiperipatus biolleyi; and a partial mitochondrial genome sequence of the Onychophora Euperipatoides kanagrensis. Tardigrada mitochondrial genomes resemble those of the arthropods in term of the gene order and strand asymmetry, whereas Onychophora genomes are characterized by numerous gene order rearrangements and strand asymmetry variations. In addition, Onychophora genomes are extremely enriched in A and T nucleotides, whereas Priapulida and Tardigrada are more balanced. Phylogenetic analyses based on concatenated amino acid coding sequences support a monophyletic origin of the Ecdysozoa and the position of Priapulida as the sister group of a monophyletic Panarthropoda (Tardigrada plus Onychophora plus Arthropoda). The position of Tardigrada is more problematic, most likely because of long branch attraction (LBA). However, experiments designed to reduce LBA suggest that the most likely placement of Tardigrada is as a sister group of Onychophora. The same analyses also recover monophyly of traditionally recognized arthropod lineages such as Arachnida and of the highly debated clade Mandibulata.

    AB - Ecdysozoa is the recently recognized clade of molting animals that comprises the vast majority of extant animal species and the most important invertebrate model organisms—the fruit fly and the nematode worm. Evolutionary relationships within the ecdysozoans remain, however, unresolved, impairing the correct interpretation of comparative genomic studies. In particular, the affinities of the three Panarthropoda phyla (Arthropoda, nychophora, and Tardigrada) and the position of Myriapoda within Arthropoda (Mandibulata vs. Myriochelata hypothesis) are among the most contentious issues in animal phylogenetics. To elucidate these relationships, we have determined and analyzed complete or nearly complete mitochondrial genome sequences of two Tardigrada, Hypsibius dujardini and Thulinia sp. (the first genomes to date for this phylum); one Priapulida, Halicryptus spinulosus; and two Onychophora, Peripatoides sp. and Epiperipatus biolleyi; and a partial mitochondrial genome sequence of the Onychophora Euperipatoides kanagrensis. Tardigrada mitochondrial genomes resemble those of the arthropods in term of the gene order and strand asymmetry, whereas Onychophora genomes are characterized by numerous gene order rearrangements and strand asymmetry variations. In addition, Onychophora genomes are extremely enriched in A and T nucleotides, whereas Priapulida and Tardigrada are more balanced. Phylogenetic analyses based on concatenated amino acid coding sequences support a monophyletic origin of the Ecdysozoa and the position of Priapulida as the sister group of a monophyletic Panarthropoda (Tardigrada plus Onychophora plus Arthropoda). The position of Tardigrada is more problematic, most likely because of long branch attraction (LBA). However, experiments designed to reduce LBA suggest that the most likely placement of Tardigrada is as a sister group of Onychophora. The same analyses also recover monophyly of traditionally recognized arthropod lineages such as Arachnida and of the highly debated clade Mandibulata.

    KW - Arthropoda

    KW - mitogenomics

    KW - long branch attraction

    KW - Tardigrada

    KW - phylogeny

    KW - strand asymmetry.

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    DO - 10.1093/gbe/evq030

    M3 - Article

    VL - 2

    SP - 425

    EP - 440

    JO - Genome Biology and Evolution

    JF - Genome Biology and Evolution

    SN - 1759-6653

    ER -