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A Cambrian–Ordovician Terrestrialization of Arachnids Lozano-Fernandez, J., Tanner, A., Puttick, M. N., Vinther, J., Edgecombe, GD., & Pisani, D. (2020). A Cambrian–Ordovician terrestrialization of arachnids. Frontiers in Genetics. https://doi.org/10.3389/fgene.2020.00182 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.3389/fgene.2020.00182 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via Frontiers at https://doi.org/10.3389/fgene.2020.00182 . Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/red/research-policy/pure/user-guides/ebr-terms/ fgene-11-00182 March 9, 2020 Time: 17:44 # 1 BRIEF RESEARCH REPORT published: 11 March 2020 doi: 10.3389/fgene.2020.00182 A Cambrian–Ordovician Terrestrialization of Arachnids Jesus Lozano-Fernandez1,2*†, Alastair R. Tanner1, Mark N. Puttick3, Jakob Vinther1,2, Gregory D. Edgecombe4* and Davide Pisani1,2* 1 School of Biological Sciences, University of Bristol, Bristol, United Kingdom, 2 School of Earth Sciences, University of Bristol, Bristol, United Kingdom, 3 Department of Biology and Biochemistry, Milner Centre for Evolution, University of Bath, Bath, United Kingdom, 4 Department of Earth Sciences, Natural History Museum, London, United Kingdom Understanding the temporal context of terrestrialization in chelicerates depends on whether terrestrial groups, the traditional Arachnida, have a single origin and whether or not horseshoe crabs are primitively or secondarily marine. Molecular dating on a Edited by: phylogenomic tree that recovers arachnid monophyly, constrained by 27 rigorously Rachel C. M. Warnock, vetted fossil calibrations, estimates that Arachnida originated during the Cambrian or ETH Zürich, Switzerland Ordovician. After the common ancestor colonized the land, the main lineages appear to Reviewed by: have rapidly radiated in the Cambrian–Ordovician boundary interval, coinciding with high Joanna Wolfe, Harvard University, United States rates of molecular evolution. The highest rates of arachnid diversification are detected David Marjanovic,´ between the Permian and Early Cretaceous. A pattern of ancient divergence estimates Leibniz Institut für Evolutions und Biodiversitätsforschung, Germany for terrestrial arthropod groups in the Cambrian while the oldest fossils are Silurian (seen *Correspondence: in both myriapods and arachnids) is mirrored in the molecular and fossil records of Jesus Lozano-Fernandez land plants. We suggest the discrepancy between molecular and fossil evidence for [email protected] terrestrialization is likely driven by the extreme sparseness of terrestrial sediments in the Gregory D. Edgecombe [email protected] rock record before the late Silurian. Davide Pisani [email protected] Keywords: Arachnida, Chelicerata, terrestrialization, Cambrian, molecular clocks, diversification †Present address: Jesus Lozano-Fernandez, Institute of Evolutionary Biology INTRODUCTION (CSIC-UPF), Barcelona, Spain Arachnids are an important group of terrestrial arthropods, including the familiar ticks, mites, Specialty section: spiders, and scorpions, together with pseudoscorpions, camel spiders, vinegaroons, whip spiders, This article was submitted to and a few other groups. Arachnids are important predatory arthropods across almost every Evolutionary and Population Genetics, conceivable terrestrial habitat. While ticks are ectoparasites that affect humans and livestock, a section of the journal spiders are ecologically the most successful arachnids and as predators consume vast quantities Frontiers in Genetics of insects. Thus, understanding when arachnids colonized land and diversified is of interest from a Received: 04 September 2019 macroevolutionary and macroecological perspective. Accepted: 14 February 2020 Arachnids are chelicerates, together with the marine horseshoe crabs (Xiphosura) and Published: 11 March 2020 sea spiders (Pycnogonida). They are the most speciose clade in Chelicerata, with more Citation: than 112,000 described extant species. Together with hexapods and myriapods, arachnids Lozano-Fernandez J, Tanner AR, represent one of three distinct and ancient events of arthropod terrestrialization (terrestrial Puttick MN, Vinther J, isopods are a younger addition to the continental arthropod biota). While arachnids Edgecombe GD and Pisani D (2020) A Cambrian–Ordovician have traditionally been considered monophyletic and terrestrial (apart from secondarily Terrestrialization of Arachnids. marine mites: Pepato et al., 2018) this picture has been challenged at different times. Front. Genet. 11:182. Scorpions were long thought to be the sister group of all other extant arachnids (Weygoldt doi: 10.3389/fgene.2020.00182 and Paulus, 1979) or most closely allied to the aquatic “sea scorpions,” the eurypterids Frontiers in Genetics| www.frontiersin.org 1 March 2020| Volume 11| Article 182 fgene-11-00182 March 9, 2020 Time: 17:44 # 2 Lozano-Fernandez et al. A Cambrian–Ordovician Terrestrialization of Arachnids (Dunlop and Webster, 1999). Early fossil scorpions have been morphological stasis, with marine stem-group representatives of interpreted as aquatic, and in some cases even as marine. Xiphosura such as Lunataspis being documented from the Late These phylogenetic hypotheses and interpretations of fossil Ordovician, ca. 445 Ma (Rudkin et al., 2008), and a species ecology have been seen as requiring independent events of from the Early Ordovician (Tremadocian) of Morocco (Van terrestrialization. Some of these views have been overturned Roy et al., 2010) extends the lineage’s history even deeper. by strong molecular (Regier et al., 2010; Sharma et al., 2014; With such a deep history revealed by the fossil record, any Sharma and Wheeler, 2014; Leite et al., 2018; Ballesteros and inferred phylogenetic position for Xiphosura within terrestrial Sharma, 2019; Lozano-Fernandez et al., 2019) and morphological arachnids would imply that the marine ecology of this lineage (Garwood and Dunlop, 2014; Klußmann-Fricke and Wirkner, should be a secondary acquisition. Although such a scenario 2016) evidence for scorpions being nested within the Arachnida is paleontologically unlikely, molecular studies have often as the sister group of the other arachnids with book lungs, the recovered horseshoe crabs in highly derived clades of arachnids, Tetrapulmonata. Indeed, detailed correspondences in book lung such as sister groups to Opiliones or Palpigradi (Pepato and morphology between scorpions and tetrapulmonates support Klimov, 2015), Ricinulei (Sharma et al., 2014; Ballesteros and their homology (Scholtz and Kamenz, 2006). The supposed Sharma, 2019), or Scorpiones and Araneae (von Reumont et al., aquatic mode of life of various fossil scorpions has also been 2012; Roeding et al., 2009; Sanders and Lee, 2010). questioned on both morphological and geological grounds As with other terrestrial groups, molecular dating has (Dunlop et al., 2008; Kühl et al., 2012). Another challenge recovered old dates for the origin and main diversification of to a single terrestrialization event in arachnids came from arachnids. As part of wider campaigns investigating arthropods analyses of phylogenomic datasets, which have often recovered using just a few arachnid representatives, Rota-Stabelli et al. the marine Xiphosura to be nested within Arachnida (Ballesteros (2013), Wheat and Wahlberg(2013), and Lozano-Fernandez and Sharma, 2019). This remains a contentious issue, as other et al.(2016) recovered dates for the origin of Arachnida with phylogenomic analyses have yielded trees in which Arachnida is credibility intervals bracketed between the Cambrian, in the first monophyletic (Lozano-Fernandez et al., 2019). two studies, and Ordovician in the latter. Recently, Ballesteros Most chelicerate lineages are predatory components of a and Sharma(2019) reported a chelicerate molecular phylogeny diverse range of ecosystems, and the rock record attests to their in which when they constrained Arachnida to be monophyletic presence in both earlier Paleozoic marine settings (Legg, 2014) inferred an Ediacaran origin for the group. Consequently, there and through into the Mesozoic and Cenozoic, which witnessed a are significant geochronological discrepancies, particularly for prolific diversification of spiders and other terrestrial arachnids terrestrial lineages, between the molecular clock-based studies (Penney, 2003; Selden et al., 2009). The terrestrial rock record and the younger dates suggested by the first appearances of fossils. prior to the Silurian is very sparse (Kenrick et al., 2012) and As fossils do not inform on the age of origin of clades (Signor has presented some apparent discordances when investigating and Lipps, 1982), but rather provide minimum ages of divergence myriapod (Fernández et al., 2018), hexapod (Lozano-Fernandez (Donoghue and Benton, 2007), clock-based methods are required et al., 2016), and plant divergence times. While the body fossil to approach an accurate evolutionary timescale. record of terrestrial plants and arthropods does not extend much Focusing on the favored topology of Lozano-Fernandez et al. further back than the Silurian (∼443–419 Ma), molecular
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