Highly diversified mitochondrial genomes provide new evidence for interordinal relationships in the Arachnida

Abstract

Arachnida is an exceptionally diverse class in the Arthropoda, consisting of 20 orders and playing crucial roles in the terrestrial ecosystems. However, their interordinal relationships have been debated for over a century. Rearranged or highly rearranged mitochondrial genomes (mitogenomes) 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 mitogenome sequences of 290 arachnid species to decipher interordinal relationships as well as diversification through time. Our results recovered monophyly of ten orders (i.e. Amblypygi, Araneae, Ixodida, Mesostigmata, Opiliones, Pseudoscorpiones, Ricinulei, Sarcoptiformes, Scorpiones and Solifugae), while rejecting monophyly of the Trombidiformes due to the unstable position of the Eriophyoidea. The monophyly of Acari (subclass) was rejected, possibly due to the long-branch attraction of the Pseudoscorpiones. The monophyly of Arachnida was further rejected because the Xiphosura nested within arachnid orders with unstable positions. Mitogenomes that are highly rearranged in mites but less rearranged or conserved in the remaining lineages point to their exceptional diversification in mite orders; however, shared derived mitochondrial (mt) gene clusters were found within superfamilies rather than interorders, confusing phylogenetic signals in arachnid interordinal relationships. Molecular dating results show that arachnid orders have ancient origins, ranging from the Ordovician to the Carboniferous, yet have significantly diversified since the Cretaceous in orders Araneae, Mesostigmata, Sarcoptiformes, and Trombidiformes. By summarizing previously resolved key positions of some orders, we propose a plausible arachnid tree of life. Our results underline a more precise framework for interordinal phylogeny in the Arachnida and provide new insights into their ancient evolution.

Mitochondrial Genomes of two Lycosa spiders (Araneae, Lycosidae): Genome Description and Phylogenetic Implications

“…All major branches in the tree were well supported by 0.526-1 BPP in BI analyses and 48-100% BS in ML analyses. In addition, the topology was very similar to those of other studies [11,34,[46][47][48][49][50].…”

“…All major branches in the tree were well supported by 0.526-1 BPP in BI analyses and 48-100% BS in ML analyses. In addition, the topology was very similar to those of other studies [11,34,[46][47][48][49][50]. According to the phylogenetic tree, the Lycosidae family was divided into two groups: the first group was recovered as (L. shanasia + L. singoriensis), and the second group was recovered as (Pirata subpiraticus + (P. laura + W. fidelis)).…”

Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae

“…This proposed remedy for long branch attraction is greatly potentiated by the availability of higher-level phylogenies for unstable groups, such as Acariformes (Klimov et al 2017) and Palpigradi (Giribet et al 2014). However, representation of solifuges in phylogenomic works has historically been driven entirely by the availability of sequence-grade tissues, rather than by phylogenetic representation, given that the internal phylogenetic structure of this order has never been fathomed (Borner et al 2014; Sharma et al 2014; Ballesteros and Sharma 2019; Arribas et al 2020; Ballesteros et al 2022; Ban et al 2022). It is possible that this oversight may have underlain their known predilection for topological instability in some phylogenomic datasets (Sharma et al 2014; Ballesteros and Sharma 2019; Ballesteros et al 2019).…”

The seven grand challenges in arachnid science

“…While morphological evidence for arachnid monophyly (i.e. Arachnida traditionally excluding Xiphosura) has once been deemed solid (Shultz, 2001;Coddington et al, 2004), most molecular studies do not recover it (Ballesteros et al, 2022;Ban et al, 2022), nor do they recover some of the classical groups within Arachnida . Monophyly and phylogenetic placement of several arachnid lineages continue to be ambiguous due to long branch attraction artifacts (Ontano et al, 2022).…”

“…The phylogenetic limits of Arachnida have yet to be precisely established (Packard, 1882;Harvey, 2002;Coddington et al, 2004;Sharma et al, 2021), but Arachnida certainly contains groups of terrestrial and aquatic chelicerates including spiders (Araneae), harvestmen (Opiliones), scorpions (Scorpiones), mites (Acariformes), ticks (Parasitiformes), pseudoscorpions (Pseudoscorpiones), camel spiders (Solifugae), whip spiders (Amblypygi), vinegaroons (Thelyphonida, also Uropygi), shorttailed whipscorpions (Schizomida), microwhip scorpions (Palpigradi), and hooded tick-spiders (Ricinulei). Arachnids also include several extinct lineages of varying ranks (Wang et al, 2018), some of them marine, and may also include the marine horseshoe crabs (Xiphosura) (Ban et al, 2022). Together, arachnid lineages comprise at least hundreds of thousands, perhaps even millions of species, of which most remain undiscovered.…”