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. 2021 May 19;38(6):2446-2467.
doi: 10.1093/molbev/msab038.

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

Andrew Z Ontano  1 , Guilherme Gainett  1 , Shlomi Aharon  2 , Jesús A Ballesteros  1 , Ligia R Benavides  3 , Kevin F Corbett  1 , Efrat Gavish-Regev  2 , Mark S Harvey  4 , Scott Monsma  5 , Carlos E Santibáñez-López  6 , Emily V W Setton  1 , Jakob T Zehms  1 , Jeanne A Zeh  7 , David W Zeh  7 , Prashant P Sharma  1
Affiliations

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

Andrew Z Ontano et al. Mol Biol Evol. .

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 long-branch attraction 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 data sets. Pseudoscorpion placement is particularly variable across data sets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount long-branch attraction, 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.

Keywords: arachnids; microRNA; ohnologs; species tree reconciliation; supermatrix.

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Figures

Fig. 1.
Fig. 1.
Summary tree topology of Chelicerata showing relationships of orders. Phylogeny based on Ballesteros et al. (2019). Dotted lines for pseudoscorpiones show alternative placements of this order in selected historical phylogenetic analyses.
Fig. 2.
Fig. 2.
Depth of taxonomic sampling is more influential than matrix completeness in supermatrix analyses of pseudoscorpion placement. (a) Internal phylogeny of Pseudoscorpiones showing major taxonomic groups. Notations on nodes indicate taxon subsets obtained by sequential pruning of branches. (b) Sensitivity plot of 42 phylogenomic matrices assembled by varying gene occupancy (y axis) and taxonomic sampling (x axis), with partitioned model-fitting. Colors of squares correspond to the sister group of Pseudoscorpiones obtained in each maximum likelihood analysis. (c) Analysis of largest (1002 loci) and densest (248 loci) matrices under variations of the PMSF model. (d) Selected tree topologies showing the dynamics of pseudoscorpion instability as a function of taxonomic sampling in partitioned-model analyses.
Fig. 3.
Fig. 3.
Depth of taxonomic sampling affects supermatrix nodal support, but not per-locus support. (a) Nodal support frequency for competing hypotheses of pseudoscorpion placement as a function of taxonomic sampling and matrix completeness. (b) Proportion of loci favoring Pseudoscorpiones + Scorpiones versus Pseudoscorpiones + either acarine order under a ΔGLS framework, as a function of taxonomic sampling and matrix completeness.
Fig. 4.
Fig. 4.
Depth of taxonomic sampling is more influential than matrix completeness in ASTRAL analyses of pseudoscorpion placement. (a) Sensitivity plot of 42 phylogenomic matrices assembled by varying gene occupancy (y axis) and taxonomic sampling (x axis). (b) Selected tree topologies showing the dynamics of pseudoscorpion instability as a function of taxonomic sampling.
Fig. 5.
Fig. 5.
Slow-evolving genes do not consistently recover Pseudoscorpiones + Scorpiones in the absence of dense taxon sampling. (a) Sensitivity plot of 21 phylogenomic matrices assembled by binning genes into tertiles of evolutionary rate (y axis) and taxonomic sampling (x axis), with partitioned model-fitting. Colors of squares correspond to the sister group of Pseudoscorpiones obtained in each maximum likelihood analysis. Above: Analyses based on the G2 family of matrices (75% complete). Below: Analyses based on the G3 family of matrices (70% complete). (b) Analyses of the corresponding data sets in (a) using ASTRAL.
Fig. 6.
Fig. 6.
Comparison of homeobox repertoires for 26 panarthropods supports retention of duplications in pseudoscorpions that are shared with arachnopulmonates. Rows correspond to individual homeobox genes. Colors correspond to numbers of paralogs. Black arrows to the right indicate duplications in at least one pseudoscorpion exemplar that is also shared by at least one arachnopulmonate.
Fig. 7.
Fig. 7.
Pseudoscorpions possess two copies of four developmental patterning genes known to exhibit paralogs with arachnopulmonate-specific spatiotemporal expression domains. Above: Single copy orthologs of dac, hth, exd, and omb were recovered from genomic resources for sea spiders, harvestmen, and Acariformes, whereas two copies of each gene were recovered for scorpions, tetrapulmonates, and pseudoscorpions. Below left: Maximum likelihood gene tree topology of the medial leg gap gene dac. Below right: Maximum likelihood gene tree topology of the proximal leg gap gene hth. Note the clustering of pseudoscorpion copies within arachnopulmonate clusters. dac-1 of C. crassus was recovered as two nonoverlapping fragments.
Fig. 8.
Fig. 8.
Hox gene complement in the pseudoscorpion genome substantiates evidence of shared WGD with other Arachnopulmonata. Columns and colored squares correspond to each Hox gene. Unfilled squares correspond to absences, not losses. Cross through abdA in T. urticae indicates loss of this Hox gene in the mite genome. Note independent 2-fold WGD events in Xiphosura (Kenny et al. 2016; Shingate et al. 2020).
Fig. 9.
Fig. 9.
Comparison of miRNA family copy number in C. scorpioides and other ecdysozoans supports retention of duplications in pseudoscorpions shared with scorpions and spiders. Columns correspond to individual miRNA families. Colors correspond to numbers of paralogs. miRNA families in red text indicate duplications in scorpions, pseudoscorpions and at least one spider. miRNA families in blue text are duplicated only in scorpions and pseudoscorpions.
Fig. 10.
Fig. 10.
Ancestral state reconstruction of shared genome duplication events and reproductive behaviors in Chelicerata, under accelerated transformation. (a) The revised placement of pseudoscorpions supports a shared origin of courtship behavior and maternal brood care across Arachnopulmonata. Empty symbols indicate absences. For book lungs, half-filled symbol for Schizomida reflects loss of posterior book lung pair; gradient in Araneae reflects transformation of posterior book lung pair to tracheal tubules in derived spiders. For promenade á deux, half-filled symbol for Pseudoscorpiones reflects retention only in Cheliferoidea. (b) A mating pair of Conicochernes crassus performing the promenade á deux (Denmark, Western Australia; photograph: A.Z. Ontano). (c) Maternal brood care in a chernetid (photograph: G. Giribet). (d) Promenade á deux behavior in the buthid scorpion Babycurus gigas (photograph: M. Cozijn). (e) Maternal care in the vaejovid scorpion Vaejovis zapoteca, with scorplings on the back of the female (photograph: C.E. Santibáñez-López). (f) Postembryos of an undescribed species of the schizomid genus Rowlandius; hatchling cluster removed from the female’s back for image clarity (photograph: L. Carvalho). (g) A mating pair of the uropygid Mastigoproctus giganteus (photograph: A. Hochberg, R. Hochberg). (h) Female of the lycosid spider Hogna sp. with spiderlings on the back of the female (photograph: J.A. Ballesteros). (i) Female of the whip spider Phrynus marginemaculatus with postembryos on the back of the female; yellow marking is a biological paint used to distinguish individuals in a captive breeding colony (photograph: G. Gainett).
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