Increasing species sampling in chelicerate genomic-scale datasets provides support for monophyly of Acari and Arachnida

Abstract

Chelicerates are a diverse group of arthropods, represented by such forms as predatory spiders and scorpions, parasitic ticks, humic detritivores, and marine sea spiders (pycnogonids) and horseshoe crabs. Conflicting phylogenetic relationships have been proposed for chelicerates based on both morphological and molecular data, the latter usually not recovering arachnids as a clade and instead finding horseshoe crabs nested inside terrestrial Arachnida. Here, using genomic-scale datasets and analyses optimised for countering systematic error, we find strong support for monophyletic Acari (ticks and mites), which when considered as a single group represent the most biodiverse chelicerate lineage. In addition, our analysis recovers marine forms (sea spiders and horseshoe crabs) as the successive sister groups of a monophyletic lineage of terrestrial arachnids, suggesting a single colonisation of land within Chelicerata and the absence of wholly secondarily marine arachnid orders.

A Cambrian–Ordovician Terrestrialization of Arachnids

“…Based on current best practice, our analysis uses fossil calibrations following the guidelines set out by Parham et al (2012) (see Table 1 and Supplementary Data Sheet S4). Furthermore, we report divergence times on a well-sampled phylogeny , using the best-fitting molecular substitution and relaxed molecular clock models (see Lozano-Fernandez et al, 2019). We therefore contend that our findings provide the currently most robust insights into early chelicerate evolution (Figure 1).…”

“…Divergence time estimation was performed using PhyloBayes 3.3f (serial version) (Lartillot et al, 2009). We fixed the topology following Lozano-Fernandez et al (2019), see previous section. We compared the fit of alternative, autocorrelated (CIR model - Lepage et al, 2006Lepage et al, , 2007 and uncorrelated (uncorrelated gamma multipliers model; UGAM -Drummond et al, 2006), relaxed molecular clock models generating ten different random splits replicates and performing crossvalidation analyses (see PhyloBayes manual for details).…”

“…Within Arachnida, we infer Acari and Arachnopulmonata do not predate the oldest body fossils of crown-group Chelicerata, using Wisangocaris barbarahardyae and its date of 509 Ma as a soft maximum following Wolfe et al (2016). The amino acid substitution model used to estimate branch lengths was the CAT-GTR + model, as in the phylogenetic analyses of Lozano-Fernandez et al (2019). All analyses were conducted using soft bounds with 5% of the probability mass outside the calibration interval.…”

“…The topology used for the molecular clock analyses here is obtained from Lozano-Fernandez et al (2019). In this tree Chelicerata and Euchelicerata are monophyletic, with the horseshoe crabs retrieved as the sister group of monophyletic Arachnida.…”

“…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).…”