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

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.