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Highly diversified mitochondrial genomes provide new evidence for inter-ordinal relationships in the Arachnida

Citation

Xue, Xiao-Feng et al. (2022), Highly diversified mitochondrial genomes provide new evidence for inter-ordinal relationships in the Arachnida, Dryad, Dataset, https://doi.org/10.5061/dryad.6hdr7sr1f

Abstract

Arachnida is an exceptionally diverse class in the Arthropoda, comprising of 20 orders and playing essential roles in the terrestrial ecosystems. However, their inter-ordinal relationships have been debated for over a century. Rearranged or highly rearranged mitochondrial (mt) genomes were consistently found in this class, but their various extent in different lineages and efficiency for resolving arachnid phylogenies are unclear. Here, we reconstructed phylogenetic trees using mt genome sequences of 290 arachnid species to decipher inter-ordinal relationships as well as diversification through time. Our results recovered monophyly of 10 orders (i.e., Amblypygi, Araneae, Ixodida, Mesostigmata, Opiliones, Pseudoscorpiones, Ricinulei, Sarcoptiformes, Scorpiones, and Solifugae), while rejected monophyly of the Trombidiformes due to unstable position of the Eriohyoidea. The monophyly of Acari (subclass) was rejected possibly due to long-branch attraction of the Pseudoscorpiones. Basal inter-ordinal relationships were partially resolved by sharing conserved mt gene arrangements. Highly rearranged mt genomes in mites while less rearranged or conserved in the remaining lineages point to their exceptionally diversification in mite orders; however, shared derived mt gene clusters were found within superfamilies rather than inter-orders, confusing phylogenetic signals in arachnid inter-ordinal relationships. Molecular dating results show that arachnid orders have ancient origins ranged from the Silurian to the Carboniferous, followed by a huge gap, crossing the Permian, Triassic, and Jurassic, then especially diversified after the Cretaceous in orders Araneae, Mesostigmata, Sarcoptiformes, and Trombidiformes. By summarizing previously resolved key positions of some orders, we propose a plausible inter-ordinal phylogeny: ((Solifugae, Palpigradi) (Phalangiotarbida (Trigonotarbida ((Uraraneida, Araneae) (Haptopoda (Amblypygi (Thelyphonida, Schizomida)))) (Opiliones (Ricinulei ((Opilioacarida (Mesostigmata (Holothyrida, Ixodida))) (Trombidiformes, Sarcoptiformes)))))) (Scorpiones, Pseudoscorpiones))). Our results underline a more precise framework for inter-ordinal phylogeny in the Arachnida and provide insights into their ancient evolution.

Funding

National Natural Science Foundation of China, Award: 31672337, 31970437

National Science and Technology Fundamental Resources Investigation Program of China, Award: 2018FY100300