A Critical Appraisal of the Placement of Xiphosura (Chelicerata) with Account of Known Sources of Phylogenetic Error

Abstract

Horseshoe crabs (Xiphosura) are traditionally regarded as sister group to the clade of terrestrial chelicerates (Arachnida). This hypothesis has been challenged by recent phylogenomic analyses, but the non-monophyly of Arachnida has consistently been disregarded as artifactual. We re-evaluated the placement of Xiphosura among chelicerates using the most complete phylogenetic data set to date, expanding outgroup sampling, and including data from whole genome sequencing projects. In spite of uncertainty in the placement of some arachnid clades, all analyses show Xiphosura consistently nested within Arachnida as the sister group to Ricinulei (hooded tick spiders). It is apparent that the radiation of arachnids is an old one and occurred over a brief period of time, resulting in several consecutive short internodes, and thus is a potential case for the confounding effects of incomplete lineage sorting (ILS). We simulated coalescent gene trees to explore the effects of increasing levels of ILS on the placement of horseshoe crabs. In addition, common sources of systematic error were evaluated, as well as the effects of fast-evolving partitions and the dynamics of problematic long branch orders. Our results indicated that the placement of horseshoe crabs cannot be explained by missing data, compositional biases, saturation, or ILS. Interrogation of the phylogenetic signal showed that the majority of loci favor the derived placement of Xiphosura over a monophyletic Arachnida. Our analyses support the inference that horseshoe crabs represent a group of aquatic arachnids, comparable to aquatic mites, breaking a long-standing paradigm in chelicerate evolution and altering previous interpretations of the ancestral transition to the terrestrial habitat. Future studies testing chelicerate relationships should approach the task with a sampling strategy where the monophyly of Arachnida is not held as the premise.

Horseshoe crab genomes reveal the evolutionary fates of genes and microRNAs after three rounds (3R) of whole genome duplication

“…Horseshoe crabs have long been regarded as a monophyletic group (Xiphosura) and the sister group to the terrestrial chelicerate clade that includes spiders and scorpions (Arachinida). However, in a recent phylogenetic analysis using publicly available data, including three xiphosurans, two pycnogonids, and 34 arachnids, it has been suggested that the horseshoe crabs represent a group of marine arachnids (Ballesteros and Sharma 2019). On the other hand, another group of researchers recovered the Xiphosura as the sister group to the Arachnida (Lorano-Fernandez et al 2019), suggesting a single terrestrialisation event occurred after the last common ancestor of arachnids and horseshoe crabs diverged.…”

Phylogenomic resolution of sea spider diversification through integration of multiple data classes

“…A list of taxa sampled from field expeditions, museum collections, and multiple deep sea cruises is provided as electronic supplementary material, table S1. Taxonomic sampling consisted of 89 sea spiders; outgroups consisted of 14 Arachnida (including one Xiphosura, which has recently been shown to be nested within the arachnids [21,22]), three Myriapoda, three Pancrustacea, and one Onychophora.…”

“…Previous efforts to decipher the higher-level relationships of sea spiders have been hindered by the omission of key lineages [11,12], inaccessibility of many families for phylotranscriptomic approaches [18,21,22], limited informativeness of legacy Sangersequenced markers [5,[11][12], compositional bias of mitochondrial genes [11], ineffectiveness of mitogenomes for resolving deep relationships of Chelicerata [13,14], and the potential for gut or epibiont contamination [5]. Here, we surmounted these challenges by integrating multiple data classes and using a target capture approach optimized for sea spider (or chelicerate) genomic sequence.…”

A Cambrian–Ordovician Terrestrialization of Arachnids

“…These phylogenetic hypotheses and interpretations of fossil ecology have been seen as requiring independent events of terrestrialization. Some of these views have been overturned by strong molecular (Regier et al, 2010;Leite et al, 2018;Ballesteros and Sharma, 2019;Lozano-Fernandez et al, 2019) and morphological (Garwood and Dunlop, 2014;Klußmann-Fricke and Wirkner, 2016) evidence for scorpions being nested within the Arachnida as the sister group of the other arachnids with book lungs, the Tetrapulmonata. Indeed, detailed correspondences in book lung morphology between scorpions and tetrapulmonates support their homology (Scholtz and Kamenz, 2006).…”