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Exploring the Evolution and Terrestrialization of Scorpions (Arachnida: Scorpiones) with Rocks and Clocks

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Exploring the Evolution and Terrestrialization of Scorpions (Arachnida: Scorpiones) with Rocks and Clocks Howard, R., Edgecombe, G. D., Legg, D., Pisani, D., & Lozano- Fernandez, J. (2019). Exploring the evolution and terrestrialization of scorpions (Arachnida: Scorpiones) with rocks and clocks. Organisms Diversity and Evolution, 19(1), 71-86. https://doi.org/10.1007/s13127- 019-00390-7 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.1007/s13127-019-00390-7 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 Springer at https://doi.org/10.1007/s13127-019-00390-7 . 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/ Organisms Diversity & Evolution (2019) 19:71–86 https://doi.org/10.1007/s13127-019-00390-7 REVIEW Exploring the evolution and terrestrialization of scorpions (Arachnida: Scorpiones) with rocks and clocks Richard J. Howard1,2,3 & Gregory D. Edgecombe2 & David A. Legg4 & Davide Pisani3 & Jesus Lozano-Fernandez5,3 Received: 3 August 2018 /Accepted: 2 January 2019 /Published online: 6 February 2019 # The Author(s) 2019 Abstract Scorpions (Arachnida: Scorpiones Koch, 1837) are an ancient chelicerate arthropod lineage characterised by distinctive subdi- vision of the opisthosoma and venomous toxicity. The crown group is represented by over 2400 extant species, and unambiguous fossil representatives are known at least from the Cretaceous Period. However, a number of extinct scorpion lineages existed in the Palaeozoic Era, many of which are of a contentious marine (or at least semi-aquatic) lifestyle, and have long caused confusion regarding the nature of arachnid terrestrialization and arachnid phylogeny more broadly. To clarify the process of terrestrialization, there is a need to marry fossil and extant scorpions in a common evolutionary framework utilising modern advances in phylogenetics. Here, we review phylogenetic hypotheses of arachnid and scorpion interrelationships, relevant advances in phylogenetic divergence time estimation and the scorpion fossil record—especially with reference to terrestrialization. In addition, we provide a list of scorpion fossil calibrations for use in molecular dating and demonstrate their utility in deriving a novel scorpion time tree using Bayesian relaxed-clock methods. Our results reveal a window of divergence from 335 to 266 Mya for the scorpion crown group, consistent with a Pangean origin of crown scorpions inferred from the biogeographical distribution of the extant fauna. Keywords Scorpions . Arachnids . Molecular clocks . Terrestrialization . Phylogenetics . Palaeobiology Introduction Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13127-019-00390-7) contains supplementary Scorpions (Arachnida: Scorpiones Koch, 1837) are a rela- material, which is available to authorized users. tively speciose (~ 2400 extant species, https://www.ntnu. no/ub/scorpion-files/) and medically significant (e.g. * Richard J. Howard Isbister and Saluba Bawaskar 2014) group of chelicerates. [email protected] The group has an almost cosmopolitan biogeographical dis- tribution, being absent only in boreal environments, 1 Department of Biosciences, University of Exeter, Stella Turk Antarctica and on some more isolated island land Building, Penryn Campus, Cornwall TR10 9TA, UK masses—though they have been translocated as anthropo- 2 Department of Earth Sciences, The Natural History Museum, genic introductions (e.g. Wanless 1977). Like most arach- Cromwell Road, London SW7 5BD, UK nids, with the exception of the more ecologically diverse 3 School of Earth Sciences and School of Biological Sciences, mites, scorpions are predators, generally feeding on other University of Bristol, Life Sciences Building, 24 Tyndall Avenue, arthropods and occasionally small vertebrates. Bristol BS8 1TQ, UK Extant scorpions are instantly recognisable in possessing a 4 School of Earth and Environmental Sciences, University of pair of chelate pincer-like pedipalps, a post-anal telson Manchester, Williamson Building, 176 Oxford Road, Manchester M13 9QQ, UK equipped with a stinger, and a pair of unique ventral comb- like sensory organs called pectines. The scorpion body plan is 5 Department of Evolutionary Biology, Ecology and Environmental Sciences and Biodiversity Research Institute (IRBio), University of also unique among arachnids with respect to its tagmosis. Barcelona, Avd. Diagonal 643, 08028 Barcelona, Spain Scorpions exhibit a clearly demarcated tripartite organisation 72 Howard R.J. et al. consisting of an anterior appendage-bearing prosoma (as in all 2014), their interrelationships are generally poorly resolved chelicerates generally), a medial mesosoma that houses the (Fig. 1), though some reasonable higher level clades are emer- reproductive and respiratory systems, and a posterior tail- gent. Tetrapulmonata—comprising Araneae, Amblypygi, like metasoma that terminates with the anus and precedes Thelyphonida, Schizomida, Uraraneida and Haptopoda; plus the telson—comprising a vesicle and aculeus via which ven- Trigonotarbida as Pantetrapulmonata (Shultz 2007)—is the om is delivered. most stable of these, with strong morphological support in Scorpions have an ancient evolutionary history, represent- the form of, among other characters, a common respiratory ed by a reasonably continuous fossil record stretching back as configuration with book lungs on the same two opisthosomal far as the Telychian Stage (Silurian, Llandovery) (Jeram 1998; segments (Shultz 1990, 2007). Multiple molecular phyloge- Dunlop 2010; Dunlop and Selden 2013; Waddington et al. netic studies have also given weight to Tetrapulmonata 2015). Scorpions therefore potentially constituted a compo- (Wheeler and Hayashi 1998; Shultz and Regier 2000; nent of the earliest faunas of complex terrestrial ecosystems, Pepato et al. 2010;Regieretal.2010; Rehm et al. 2012; along with myriapods and, at least by the Early Devonian, Sharma et al. 2014), and the most recent and data-rich of these hexapods (see Lozano-Fernandez et al. 2016). Little has been studies have allied this group to scorpions. Using different done however to constrain the radiation of the extant and fossil multilocus and phylogenomic-scale datasets Regier et al. scorpion lineages together in a common evolutionary frame- (2010) and Sharma et al. (2014) each recovered a sister group work. This is unfortunate as the evolutionary radiation(s) of relationship between Tetrapulmonata and Scorpiones. Sharma scorpions is of interest in the study of arthropod macroevolu- et al. (2014) renamed this clade Arachnopulmonata, replacing tion and biogeography, terrestrialization (both from a physio- the earlier Pulmonata (Firstman 1973) to avoid confusion with logical perspective and in the context of the evolution of the the clade of terrestrial molluscs of the same name. Scorpions, Earth system), and in resolving the problematic phylogenetic like tetrapulmonates, possess book lungs, whereas all other relationships between the arachnid orders. arachnids have non-pulmonate respiratory systems (typically As such, we aim to provide an interdisciplinary synthesis tracheae); and comparative study of scorpion and on scorpion evolution by reviewing modern and historical tetrapulmonate book lungs has revealed detailed structural phylogenetic hypotheses of scorpion interrelationships, and similarities that are consistent with them being homologous scorpion palaeontology—framed within the context of arach- (Scholtz and Kamenz 2006). Likewise, comparative work on nid terrestriality. We highlight the complementary nature of the tetrapulmonate and scorpion vascular systems has implied scorpions to critically evaluate molecular dating studies, and homology (Klußmann-Fricke and Wirkner 2016). provide additional fossil calibrations for dating the scorpion Furthermore, it has been identified that scorpions and spiders Tree of Life. In addition, we apply these fossil calibrations in a share a common ancestral whole genome duplication that is Bayesian relaxed-clock analysis in order to constrain the age present in all arachnopulmonates, therefore being an addition- of the scorpion crown group. al line of evidence suggesting the monophyly of the group (Leite et al. 2018). Previous phylogenetic hypotheses based on morphology Scorpions on the arachnid Tree of Life have posited scorpions in a range of positions on the chelicerate tree including (I) sister group to the remaining Within the Chelicerata, scorpions belong to the familiar group Arachnida (Weygoldt and Paulus 1979); (II) not arachnids Arachnida, the systematic origin of which can be traced back at all, but closer to eurypterids (sea scorpions) (Dunlop and to the nineteenth century French naturalist Jean-Baptiste Braddy 2001); and (III) distant from the tetrapulmonates but Lamarck (Lamarck 1801). In its modern iteration, Arachnida within Arachnida, allied with Opiliones (Shultz 1990, 2007; usually comprises 16 orders. These include the living Wheeler and Hayashi 1998; Giribet et al. 2002). Hypothesis Scorpiones (true scorpions), Pseudoscorpiones (pseudoscor- 1(Fig.2a) and hypothesis 3 (Fig. 2c) imply that the seem- pions or false
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