Comprehensive Species Sampling and Sophisticated Algorithmic Approaches Refute the Monophyly of Arachnida

Abstract

Deciphering the evolutionary relationships of Chelicerata (arachnids, horseshoe crabs, and allied taxa) has proven notoriously difficult, due to their ancient rapid radiation and the incidence of elevated evolutionary rates in several lineages. While conflicting hypotheses prevail in morphological and molecular datasets alike, the monophyly of Arachnida is nearly universally accepted, despite historical lack of support in molecular datasets. Some phylotranscriptomic analyses have recovered arachnid monophyly, but these did not sample all living orders, whereas analyses including all orders have failed to recover Arachnida. To understand this conflict, we assembled a dataset of 506 high-quality genomes and transcriptomes, sampling all living orders of Chelicerata with high occupancy and rigorous approaches to orthology inference. Our analyses consistently recovered the nested placement of horseshoe crabs within a paraphyletic Arachnida. This result was insensitive to variation in evolutionary rates of genes, complexity of the substitution models, and alternative algorithmic approaches to species tree inference. Investigation of sources of systematic bias showed that genes and sites that recover arachnid monophyly are enriched in noise and exhibit low information content. To test the impact of morphological data, we generated a 514-taxon morphological data matrix of extant and fossil Chelicerata, analyzed in tandem with the molecular matrix. Combined analyses recovered the clade Merostomata (the marine orders Xiphosura, Eurypterida, and Chasmataspidida), but merostomates appeared nested within Arachnida. Our results suggest that morphological convergence resulting from adaptations to life in terrestrial habitats has driven the historical perception of arachnid monophyly, paralleling the history of numerous other invertebrate terrestrial groups.

Parallel duplication and loss of aquaporin-coding genes during the ‘out of the sea’ transition as potential key drivers of animal terrestrialization

“…On the contrary, Pycnogonida, the earliest-splitting chelicerate lineage, has retained both copies. This is consistent with a single terrestrialization event in arachnids (considering a secondary later colonisation of water by xiphosurans as discussed in (Ballesteros et al 2022)), where the duplication of Aqp3-like may have helped chelicerates to transition to a different niche. We could hypothesise that this new copy might have replaced the ancient Aqp3-like if it were neo- or subfunctionalized into a more efficient transporter, as reported with other aquaporins (Finn et al 2015).…”

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

“…Fossil orders Trigonotarbida and Uraraneida were thought to be sister groups to Araneae (Garwood et al., 2014; Howard et al., 2020; Shultz, 2007), and fossil order Haptopoda was the sister group of Pedipalpi (Dunlop, 1999; Shultz, 2007). The phylogenetic position of fossil order Phalangiotarbida remains unresolved but was potentially suggested close to Tetrapulmonata by sharing a prosomal sternite with distinct sclerites (Pollitt et al., 2004) or as the sister group of Opiliones by total evidence of morphological characters and slowly evolving genes (Ballesteros et al., 2022). Pseudoscorpiones was resolved as the sister group to Scorpiones by multiple lines of evidence (Ontano et al., 2021; Sharma et al., 2014).…”

“…Under this scheme, we suggest that the Solifugae may be located at the base of the arachnid tree of life. Solifugae was suggested as the sister group to Acariformes (Ballesteros et al., 2022; Pepato & Klimov, 2015; Pepato et al., 2010), whereas Palpigradi was the sister group to clade Solifugae + Acariformes (Ballesteros et al., 2022; Pepato et al., 2010).…”

The rediscovery of a relict unlocks the first global phylogeny of whip spiders (Amblypygi)

“…Outgroup sampling leveraged previous phylogenomic works that have established Amblypygi as the sister group of vinegaroons (Thelyphonida), and short-tailed whip scorpions (Schizomida) (the clade Pedipalpi; Sharma et al 2014; Ballesteros and Sharma 2019; Ballesteros et al 2019). Pedipalpi in turn is understood to form a clade with spiders, scorpions, and pseudoscorpions, a relationship supported by rare genomic changes (e.g., Ontano et al 2021, 2022; Ballesteros et al 2022). We therefore included two representatives of spiders, one vinegaroon, three Schizomida, and rooted the tree with three scorpions.…”