How many long branch orders occur in Chelicerata? Opposing effects of Palpigradi and Opilioacariformes on phylogenetic stability

Ontano, Andrew Z; Steiner, Hugh G.; Sharma, Prashant P.

doi:10.1016/j.ympev.2021.107378

Cited by 13 publications

(15 citation statements)

References 51 publications

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“…1). However, in light of the latest evidence from phylogenomic studies Lozano-Fernandez et al, 2019;Ontano et al, 2021Ontano et al, , 2022Sharma et al, 2014) as well as our inferred topologies and mt gene arrangements, we propose a plausible arachnid tree of life (Fig. 3).…”

Section: Interordinal Relationships Within Arachnidasupporting

confidence: 57%

“…The discrepancies for arachnid interordinal relationships inferred by morphological characters or molecular approaches are likely caused by incomplete lineage sorting (Ballesteros & Sharma, 2019), long‐branch attraction of Pseudoscorpiones, Acariformes, Palpigradi and Parasitiformes (Arabi et al., 2012; Ballesteros & Sharma, 2019; Ontano et al., 2021, 2022; Pepato et al., 2010; Sharma et al., 2014), or the ancient rapid radiation of orders (Dunlop & Selden, 2009). Nevertheless, several interordinal relationships have been resolved: (1) Pseudoscorpiones is the sister group to Scorpiones by evidence from both morphological synapomorphies and genome architectures (Ontano et al., 2021), (2) sharing a genome duplication unites the Tetrapulmonata and Panscorpiones (sensu Ontano, et al., 2021), and (3) the monophyly of Acariformes and Parasitiformes was consistently recovered by genomic‐scale analyses (Ontano et al., 2022; Xue et al., 2017). However, the arachnid tree of life covering all orders remains unstable.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2022

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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.

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Section: Interordinal Relationships Within Arachnidasupporting

confidence: 57%

Section: Introductionmentioning

confidence: 99%

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

et al. 2022

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“…As anticipated, several groups in our phylogeny reflected long root-to-tip distances, constituting lineages prone to LBA artifacts. The inclusion of Opilioacariformes, a slowly evolving group of Parasitiformes ( Klompen et al 2007 ; Pepato et al 2010 ), was recently shown to break up the grouping of Acariformes and Parasitiformes, suggesting that Acari is a long-branch artifact ( Ontano et al 2021 ; Ontano et al 2022 ). In this study, we sampled Opilioacariformes with two libraries, and concordantly, never obtained the monophyly of Acari, particularly when pursuing approaches best suited to mitigating LBA ( fig.…”

Section: Discussionmentioning

confidence: 99%

“…In tandem with such approaches, investigations of chelicerate phylogeny should emphasize the expansion of whole-genome data sets, with the aim of leveraging rare genomic changes, such as genome duplications, as potential arbiters of competing phylogenetic hypotheses ( Schwager et al 2017 ). This strategy has shown strong promise as a source of benchmarks for assessing performance of molecular data sets in the face of LBA, as well as for realigning interpretations of morphological data, toward reconciliation of chelicerate relationships ( Ontano et al 2021 ; Ontano et al 2022 ).…”

Section: Discussionmentioning

confidence: 99%

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

Ballesteros

Santibáñez‐López

Baker

et al. 2022

Molecular Biology and Evolution

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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.

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“…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.…”

Section: Methodsmentioning

confidence: 99%

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

Miranda

Kulkarni

Tagliatela

et al. 2022

Preprint

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Asymmetrical rates of cladogenesis and extinction abound in the Tree of Life, resulting in numerous minute clades that are dwarfed by larger sister groups. Such taxa are commonly regarded as phylogenetic relicts or “living fossils” when they exhibit an ancient first appearance in the fossil record and prolonged external morphological stasis, particularly in comparison to their more diversified sister groups. Due to their special status, various phylogenetic relicts tend to be well-studied and prioritized for conservation. A notable exception to this trend is found within Amblypygi (“whip spiders”), a visually striking order of functionally hexapodous arachnids that are notable for their antenniform first walking leg pair (the eponymous “whips”). Paleoamblypygi, the putative sister group to the remaining Amblypygi, is known from Late Carboniferous and Eocene deposits, but is survived by a single living species, Paracharon caecus Hansen, 1921, that was last collected in 1899. Due to the absence of genomic sequence-grade tissue for this vital taxon, there is no global molecular phylogeny for Amblypygi to date, nor a fossil-calibrated estimation of divergences within the group. Here, we report several individuals of a previously unknown species of Paleoamblypygi from a cave site in Colombia. Capitalizing upon this discovery, we generated the first molecular phylogeny of Amblypygi, integrating ultraconserved element sequencing with legacy Sanger datasets and including described extant genera. To quantify the impact of sampling Paleoamblypygi on divergence time estimation, we performed in silico experiments with pruning of Paracharon. We demonstrate that the omission of relicts has a significant impact on the accuracy of node dating approaches that outweighs the impact of excluding ingroup fossils. Our results underscore the imperative for biodiversity discovery efforts in elucidating the phylogenetic relationships of “dark taxa”, and especially phylogenetic relicts in tropical and subtropical habitats.

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How many long branch orders occur in Chelicerata? Opposing effects of Palpigradi and Opilioacariformes on phylogenetic stability

Cited by 13 publications

References 51 publications

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

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

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

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

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