Phylogenomic interrogation of arachnida reveals systemic conflicts in phylogenetic signal

  • Sharma P
  • Kaluziak S
  • Pérez-Porro A
 et al. 
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Chelicerata represents one of the oldest groups of arthropods, with a fossil record extending to the Cambrian, and is sister to the remaining extant arthropods, the mandibulates. Attempts to resolve the internal phylogeny of chelicerates have achieved little consensus, due to marked discord in both morphological and molecular hypotheses of chelicerate phylogeny. The monophyly of Arachnida, the terrestrial chelicerates, is generally accepted, but has garnered little support from molecular data, which have been limited either in breadth of taxonomic sampling or depth of sequencing. To address the internal phylogeny of this group, we employed a phylogenomic approach, generating transcriptomic data for 17 species in combination with existing data, including two complete genomes. We analyzed multiple datasets containing up to 1,235,912 sites across 3,644 loci, using alternative approaches to optimization of matrix composition. Here we show that phylogenetic signal for the monophyly of Arachnida is restricted to the 500 slowest-evolving genes in the dataset. Accelerated evolutionary rates in the orders Acariformes, Pseudoscorpiones, and Parasitiformes potentially engender long-branch attraction artifacts, yielding non-monophyly of Arachnida with increasing support upon incrementing the number of concatenated genes. Mutually exclusive hypotheses are supported by locus groups of variable evolutionary rate, revealing significant conflicts in phylogenetic signal. Analyses of gene-tree discordance indicate marked incongruence in relationships among chelicerate orders, whereas derived relationships are demonstrably robust. Consistently recovered and supported relationships include the monophyly of Chelicerata, Euchelicerata, Tetrapulmonata, and all orders represented by multiple terminals. Relationships supported by subsets of slow-evolving genes include Ricinulei + Solifugae; a clade comprised of Ricinulei, Opiliones, and Solifugae; and a clade comprised of Tetrapulmonata, Scorpiones, and Pseudoscorpiones. We demonstrate that outgroup selection without regard for branch length distribution exacerbates long branch attraction artifacts and does not mitigate gene-tree discordance, regardless of high gene representation for outgroups that are model organisms. Arachnopulmonata (new name) is proposed for the clade comprising Scorpiones + Tetrapulmonata (previously named Pulmonata).

Author-supplied keywords

  • Arthropoda
  • ancient rapid radiation
  • arachnids
  • concatenation
  • orthology prediction
  • topological conflict
  • transcriptomics

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  • Stefan T. Kaluziak

  • Alicia R. Pérez-Porro

  • Vanessa L. González

  • Gustavo Hormiga

  • Ward C. Wheeler

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