Taxonomic Sampling and Rare Genomic Changes Overcome Long-Branch Attraction in the Phylogenetic Placement of Pseudoscorpions

Abstract

Long-branch attraction is a systematic artifact that results in erroneous groupings of fast-evolving taxa. The combination of short, deep internodes in tandem with LBA artifacts has produced empirically intractable parts of the Tree of Life. One such group is the arthropod subphylum Chelicerata, whose backbone phylogeny has remained unstable despite improvements in phylogenetic methods and genome-scale datasets. Pseudoscorpion placement is particularly variable across datasets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount LBA, we investigated the effect of taxonomic sampling via sequential deletion of basally branching pseudoscorpion superfamilies, as well as varying gene occupancy thresholds in supermatrices. We show that concatenated supermatrices and coalescent-based summary species tree approaches support a sister group relationship of pseudoscorpions and scorpions, when more of the basally branching taxa are sampled. Matrix completeness had demonstrably less influence on tree topology. As an external arbiter of phylogenetic placement, we leveraged the recent discovery of an ancient genome duplication in the common ancestor of Arachnopulmonata as a litmus test for competing hypotheses of pseudoscorpion relationships. We generated a high-quality developmental transcriptome and the first genome for pseudoscorpions to assess the incidence of arachnopulmonate-specific duplications (e.g., homeobox genes and miRNAs). Our results support the inclusion of pseudoscorpions in Arachnopulmonata (new definition), as the sister group of scorpions. Panscorpiones (new name) is proposed for the clade uniting Scorpiones and Pseudoscorpiones.

Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates

“…opilio exhibited no duplication of any Hox genes, in line with previous genomic surveys ( Leite et al 2018 ; Gainett et al 2021 ). In the mite T. urticae , we did not identify Hox3 and abdA candidates, consistent with Grbić et al (2011) and Ontano et al (2021) . The resolution of several sequences from T. urticae was variable; for example, previously identified Tu-ftz-1 , Tu-ftz-2 , Tu-AbdB , and Tu-Ubx sequences ( Grbić et al 2011 ) did not resolve correctly in the full Hox tree ( Figure 2 ) but did in the homeodomain and homeobox trees (Supplementary Files S5–S8).…”

“…However, data are only available for a handful of species so far, resulting in very patchy taxonomic sampling. For example, only P. tepidariorum , Pholcus phalangioides and recently, Aphonopelma hentzi , have been comprehensively surveyed for homeobox genes among spiders ( Leite et al 2018 ; Ontano et al 2021 ), omitting the large and derived retrolateral tibial apophysis (RTA) clade, which includes jumping spiders, crab spiders, and other free hunters, and the systematic identification of Wnt genes has been restricted to only P. tepidariorum . Spiders and scorpions are by far the most speciose of the arachnopulmonates, and there may be additional diversity in their repertoires of these important developmental gene families of which we are not yet aware.…”

“…Particularly given the derived nature of their appendages, this group could shed substantial light on genomic and morphological evolution following WGD. The position of pseudoscorpions was also recently resolved within Arachnopulmonata, complemented by widespread homeobox gene duplication ( Ontano et al 2021 ).…”

Tales of schizomid tails: patterns in schizomid flagellum shape from elliptical Fourier analysis

“…Schizomids are classified into two families -Protoschizomidae and Hubbardiidae -which together are the sister lineage of the larger, better known thelyphonids, colloquially called vinegaroons or whip scorpions. This relationship between schizomids and thelyphonids has been established morphologically 5,6 and recently corroborated by highthroughput molecular analyses [7][8][9][10][11] . Relationships within Schizomida are recently being better understood, with phylogenetic analyses focusing on specific clades (e.g.…”

Take a deep breath… The evolution of the respiratory system of symphytognathoid spiders (Araneae, Araneoidea)

“…Book lungs seem to be structurally homologous within pulmonated Arachnida (Scholtz & Kamenz, 2006), and their presence is a synapomorphy of Arachnopulmonata (Sharma et al, 2014;Scorpiones, Araneae, Pedipalpi, and most likely Schizomida). Recent genomic studies (Ontano et al, 2021) have enlarged the composition of Arachnopulmonata by supporting a sistergroup relationship between Scorpiones and Pseudoscorpiones (a lineage now known as Panscorpiones) in which case the absence of book lungs in pseudoscorpions is inferred to be secondary (that is, the book lungs are lost).…”