Arachnid monophyly: Morphological, palaeontological and molecular support for a single terrestrialization within Chelicerata

https://doi.org/10.1016/j.asd.2020.100997Get rights and content

Highlights

  • Arachnids are ancestrally terrestrial or amphibious, and probably lacked gnathobasic feeding, compound eyes and book gills.

  • It is unlikely that scorpions originated in aquatic environments.

  • A highly complete molecular matrix of 200 slowly evolving genes with diverse taxon sampling yields Arachnida without model-dependency.

  • Arachnids colonised land and diversified in the Cambrian–Ordovician.

Abstract

The majority of extant arachnids are terrestrial, but other chelicerates are generally aquatic, including horseshoe crabs, sea spiders, and the extinct eurypterids. It is necessary to determine whether arachnids are exclusively descended from a single common ancestor (monophyly), because only that relationship is compatible with one land colonisation in chelicerate evolutionary history. Some studies have cast doubt on arachnid monophyly and recast the origins of their terrestrialization. These include some phylogenomic analyses placing horseshoe crabs within Arachnida, and from aquatic Palaeozoic stem-group scorpions. Here, we evaluate the possibility of arachnid monophyly by considering morphology, fossils and molecules holistically. We argue arachnid monophyly obviates the need to posit reacquisition/retention of aquatic characters such as gnathobasic feeding and book gills without trabeculae from terrestrial ancestors in horseshoe crabs, and that the scorpion total-group contains few aquatic taxa. We built a matrix composed of 200 slowly-evolving genes and re-analysed two published molecular datasets. We retrieved arachnid monophyly where other studies did not - highlighting the difficulty of resolving chelicerate relationships from current molecular data. As such, we consider arachnid monophyly the best-supported hypothesis. Finally, we inferred that arachnids terrestrialized during the Cambrian–Ordovician using the slow-evolving molecular matrix, in agreement with recent analyses.

Introduction

Chelicerata is an ancient and highly diverse clade, representing one of the two subphyla of Arthropoda (its counterpart being Mandibulata, containing myriapods and pancrustaceans). Discerning whether there was a single terrestrial common ancestor of the extant terrestrial chelicerates (Arachnida – spiders, scorpions, mites, ticks, etc.) is an intriguing question in arthropod macroevolution and palaeobiology. This is because it allows an inference of how many terrestrialization events there are likely to have been in chelicerate evolutionary history - one vs. multiple (Scholtz and Kamenz, 2006). The answer to that question is pertinent because arachnids are among the most numerous and diverse land animals, and therefore their adaptation to living on land is of great evolutionary interest.

Among extant Chelicerata, three subclades are traditionally recognised: the marine sea spiders (Pycnogonida) and horseshoe crabs (Xiphosura), and the terrestrial Arachnida. Arachnida and Xiphosura, along with the fossil groups Eurypterida, Chasmataspidida and “synziphosurines” – the latter a polyphyletic assemblage of horseshoe crab-like forms (Lamsdell, 2013, 2016) – are grouped together as Euchelicerata. Synziphosurines are resolved in the stem groups of Xiphosura and Dekatriata (the proposed arachnid-eurypterid-chasmataspidid clade), as well as some of the most basal branches within Euchelicerata (Lamsdell, 2013, 2016). Most studies indicate that Pycnogonida and Euchelicerata are sister taxa (Giribet, 2018), and that Euchelicerata is monophyletic – even when more stemward Cambrian chelicerate fossils are analysed (Legg et al., 2013; Aria & Caron, 2017, 2019). Exceptionally preserved stem-group chelicerates and/or stem-group euchelicerates (depending on the relative position of Pycnogonida, which is problematic to resolve due to a highly autapomorphic bodyplan) from Cambrian Konservat-Lagerstätten include Sanctacaris uncata (Briggs and Collins, 1988; Legg, 2014), Habelia optata (Aria and Caron, 2017) and Mollisonia plenovenatrix (Aria and Caron, 2019) from the Burgess Shale.

The phylogenetic relationships between extant euchelicerates have proved highly problematic to resolve by morphology and molecules alike – particularly the relationships between the arachnid orders (Wheeler and Hayashi, 1998; Giribet et al., 2002; Shultz, 2007; Regier et al., 2010; Sharma et al., 2014; Giribet, 2018; Ballesteros and Sharma, 2019; Lozano-Fernandez et al., 2019; Ballesteros et al., 2019). This presents a great challenge when reconstructing the history of chelicerate terrestrialization, because the inferences of historic land colonisations in any group of animals are dependent on the branching order of the evolutionary tree. Conflicting phylogenetic hypotheses can confound the position of nodes representing a shift to a terrestrial lifestyle, which has led to ambiguity regarding how many terrestrialization events have occurred in Chelicerata. As all living arachnids are terrestrial – bar a few obviously secondarily aquatic groups such as the marine and freshwater mites (Pepato et al., 2018) – it is traditionally inferred that they could have originated from a terrestrial ancestor if they are monophyletic. As this common ancestor is unknown, support for this hypothesis relies on the identification of apomorphic characters for monophyletic Arachnida that are demonstrably adaptations to a terrestrial lifestyle (Scholtz and Kamenz, 2006). However, it has been argued that this is an overly simplistic line of reasoning (Shultz, 2007). This is due to the difficulties in discriminating such characters as exclusively associated with terrestrial taxa, the possibility of convergent evolution, as well as the assumption of a dichotomy between aquatic and terrestrial living - as opposed to the amphibiousness seen in horseshoe crabs, eurypterids (Lamsdell et al., 2020), and various pancrustaceans. Furthermore, arachnid monophyly has been questioned historically (see review in Giribet, 2018), but particularly more recently (Ballesteros and Sharma, 2019), which fully opens up the possibility that there have been cases of independent terrestrialization among different arachnid groups.

Morphology-based phylogenetic analyses generally support arachnid monophyly (Wheeler and Hayashi, 1998; Giribet et al., 2002; Shultz, 2007; Legg et al., 2013; Garwood and Dunlop, 2014a), and substantial lists of morphological autapomorphies have been proposed to support Arachnida, e.g., 11 characters listed by Shultz (2001). However, in explicit analyses of morphological datasets, arachnid monophyly is sometimes based on only a few apomorphic characters (Garwood and Dunlop, 2014a); or by effectively assuming arachnid monophyly by rooting the trees between Xiphosura and Arachnida (Shultz, 2007); or by sampling only a subset of crown group arachnid diversity, such that arachnid monophyly was not severely tested (Lamsdell, 2013, 2016). Some palaeontological studies contested arachnid monophyly by allying scorpions with eurypterids, but this relationship was either not based on an explicit optimality criterion (Selden and Jeram, 1989; Dunlop and Webster, 1999) or was in fact found to be unparsimonious (Dunlop and Braddy, 2001). More serious challenges to arachnid monophyly have come from molecular datasets (Sharma et al., 2014; Pepato and Klimov, 2015; Ballesteros and Sharma, 2019; Ballesteros et al., 2019; Noah et al., 2020). Molecular evidence has been presented recently to support a derived position of the marine Xiphosura within the terrestrial arachnid lineages (Ballesteros and Sharma, 2019; Ballesteros et al., 2019; Noah et al., 2020) - with some topologies suggesting lung-bearing arachnids (Arachnopulmonata - e.g. scorpions and spiders) could have terrestrialized from xiphosuran-like ancestors independently of apulmonate arachnid groups (e.g. Acari, Opiliones, Solifugae, etc.). However, another recent molecular study has on the contrary supported arachnid monophyly and suggested that placement of xiphosurans within Arachnida could be artefactual (Lozano-Fernandez et al., 2019). Another source of controversy comes from the presumptive aquatic nature of some stem-group scorpions (Dunlop et al., 2008; Poschmann et al., 2008; Kühl et al., 2012; Dunlop and Selden, 2013; Waddington et al., 2015; Wendruff et al., 2020), which may imply scorpions invaded terrestrial environments independently of other arachnids - regardless of the phylogenetic position of Xiphosura. As such, there are clear issues impeding inferences of chelicerate terrestrial evolutionary history that require clarification.

Within the context of this special issue – arthropod terrestrialization – we critically discuss the possibility of a monophyletic Arachnida and a single land colonisation in Chelicerata. Approaching the question holistically, we consider both fossil/morphological data and molecular sequence data. We discuss four key morphological character systems that bear significance for chelicerate terrestrialization. These include 1) the occurrence of gnathobasic feeding in horseshoe crabs, aquatic fossil chelicerates, and relevant outgroups, 2) the reduction of the compound lateral eye in arachnids, 3) the homology and occurrence of lamellate respiratory structures in euchelicerates (book gills and book lungs), 4) the aquatic origin of the scorpion total-group. From a molecular standpoint, we built a molecular matrix based on 200 slowly evolving genes and re-analysed two molecular datasets, from Regier et al. (2010) and Sharma et al. (2014), that recovered Xiphosura within a paraphyletic Arachnida in recently published studies - in Noah et al. (2020) and Ballesteros and Sharma (2019) respectively. In contrast to the original studies, we recover arachnid monophyly from each matrix and discuss the reasons for this discordance. We conclude that the difficulty in resolving arachnid phylogeny from current molecular datasets justifies precedence to morphological arguments for the monophyly of Arachnida.

Section snippets

The significance of gnathobasic feeding

Some of the most significant differences between the appendages of arachnids and xiphosurans involve the structure and function of the coxa in feeding, specifically whether or not a series of prosomal coxae bears a row of spinose projections known as gnathobases, and whether or not the coxa-body joint is mobile. Gnathobases are masticatory endites of the protopodite/coxa (and, in fossils, sometimes additional podomeres of the endopodite/telopodite distal to the protopodite) of a range of

Previous research on arachnid systematics

As noted above, morphological systematics of Chelicerata has generally recovered arachnid monophyly (Weygoldt and Paulus, 1979; Shultz, 2007; Garwood and Dunlop, 2014a; Legg et al., 2013; Aria and Caron, 2017, 2019), albeit with the relationships between arachnid orders largely in discordance apart from monophyly of Tetrapulmontata. Early attempts at combining morphological characters and a few molecular markers resulted in mixed hypotheses, either supporting Arachnida (Wheeler and Hayashi, 1998

Conclusions

All phylogenomic placements of Xiphosura within a paraphyletic Arachnida have put Xiphosura in a derived position, for example as sister clade to Ricinulei or Arachnopulmonata. As such, there can be two interpretations of the morphological characters exhibited by Xiphosura that are shared by fossil marine total-group chelicerates but not by arachnids - such as the spinose prosomal gnathobase series, compound eyes and non-trabeculate book gills (see sections 2.1–2.3). One scenario is that

Funding

RJH was supported by the NERC GW4+ doctoral training partnership. JL-F was supported by a Marie Skłodowska-Curie Fellowship (655814), a Palaeontological Association grant (PA-RG201701MP), and postdoctoral contract funded by the Beatriu de Pinós Programme of the Generalitat de Catalunya (2017-BP-00266). MNP and was funded by the Royal Commission for the Exhibition of 1851.

Research data

Data matrices, gene trees and alignments, output files, and custom scripts can be found in the Figshare data repository at https://figshare.com/projects/Arachnida_ASD/84527.

Author’s contribution

Richard J. Howard: Conceptualization; Investigation; Methodology; Visualization; Writing - original draft; Writing - review & editing; Mark N. Puttick: Formal analysis; Methodology; Software; Writing - original draft; Gregory D. Edgecombe: Conceptualization; Investigation; Supervision; Writing - original draft; Writing - review & editing; Jesus Lozano-Fernandez: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Software; Visualization; Writing - original draft;

Acknowledgements

This manuscript was improved by the suggestions of two anonymous reviewers, and Nicolás Mongiardino Koch provided help and discussion on the molecular phylogenetic component of this study. This project was delayed by the 2020 covid-19 pandemic lockdowns of the United Kingdom and Spain.

References (103)

  • A.R. Pepato et al.

    Molecular phylogeny of marine mites (Acariformes: Halacaridae), the oldest radiation of extant secondarily marine animals

    Mol. Phylogenet. Evol.

    (2018)
  • G. Scholtz et al.

    The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): evidence for homology and a single terrestrialisation event of a common arachnid ancestor

    Zoology

    (2006)
  • N.J. Strausfeld et al.

    Arthropod eyes: the early Cambrian fossil record and divergent evolution of visual systems

    Arthropod Struct. Dev.

    (2016)
  • W.C. Wheeler et al.

    The phylogeny of the extant Chelicerate orders

    Cladistics

    (1998)
  • R.P. Anderson et al.

    What big eyes you have: the ecological role of giant pterygotid eurypterids

    Biol. Lett.

    (2014)
  • C. Aria et al.

    Mandibulate convergence in an armoured Cambrian stem chelicerate

    BMC Evol. Biol.

    (2017)
  • C. Aria et al.

    A middle Cambrian arthropod with chelicerae and proto-book gills

    Nature

    (2019)
  • J.A. Ballesteros et al.

    A new orthology assessment method for phylogenomic data: unrooted phylogenetic orthology

    Mol. Biol. Evol.

    (2016)
  • J.A. Ballesteros et al.

    A critical appraisal of the placement of Xiphosura (Chelicerata) with account of known sources of phylogenetic error

    Syst. Biol.

    (2019)
  • J.A. Ballesteros et al.

    Ordered phylogenomic subsampling enables diagnosis of systematic errors in the placement of the enigmatic arachnid order Palpigradi

    Proc. Roya. Soc. B

    (2019)
  • R.D.C. Bicknell et al.

    Computational biomechanical analyses demonstrate similar shell-crushing abilities in modern and ancient arthropods

    Proc. Roya. Soc. B

    (2018)
  • R.D.C. Bicknell et al.

    New insights into the evolution of lateral compound eyes in Palaeozoic horseshoe crabs

    Zool. J. Linn. Soc.

    (2019)
  • S.J. Braddy et al.

    Lamellate book-gills in a late Ordovician eurypterid from the Soom Shale, South Africa: support for a eurypterid-scorpion clade

    Lethaia

    (1999)
  • D.E.G. Briggs et al.

    A middle Cambrian chelicerate from Mount Stephen, British Columbia

    Palaeontology

    (1988)
  • Z. Di et al.

    Homeosis in a scorpion supports a telopodal origin of pectines and components of the book lungs

    BMC Evol. Biol.

    (2018)
  • M. dos Reis et al.

    Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times

    Mol. Biol. Evol.

    (2011)
  • E. Draganits et al.

    A Gondwanan coastal arthropod ichnofauna from the Muth Formation (Lower Devonian, Northern India): paleoenvironment and tracemaker behaviour

    Palaios

    (2001)
  • J.A. Dunlop et al.

    Scorpions and their sister-group relationships

  • J.A. Dunlop et al.

    Scorpion fragments from the Silurian of Powys, Wales

    Arachnology

    (2013)
  • J.A. Dunlop et al.

    Fossil evidence, terrestrialization and arachnid phylogeny

    J. Arachnol.

    (1999)
  • J.A. Dunlop et al.

    Reinterpretation of the silurian scorpions Proscorpius osbornis (Whitfield): integrating data from palaeozoic and recent scorpions

    Palaeontology

    (2008)
  • R.D. Farley

    The ultrastructure of book lung development in the bark scorpion Centruroides gracilis (Scorpiones: Buthidae)

    Front. Zool.

    (2011)
  • R.D. Farley

    Ultrastructure of book gill development in embryos and first instars of the horseshoe crab Limulus polyphemus L. (Chelicerata, Xiphosura)

    Front. Zool.

    (2012)
  • S.R. Fayers et al.

    A new early devonian trigonotarbid arachnid from the Windyfield Chert, Rhynie, Scotland

    J. Syst. Palaeontol.

    (2005)
  • B. Firstman

    The relationship of the chelicerate arterial system to the evolution of the endosternite

    J. Arachnol.

    (1973)
  • R.J. Garwood et al.

    Morphology and systematics of Anthracomartidae (Arachnida: Trigonotarbida)

    Palaeontology

    (2011)
  • R.J. Garwood et al.

    Three-dimensional reconstruction and the phylogeny of extinct chelicerate orders

    PeerJ

    (2014)
  • R.J. Garwood et al.

    The Walking Dead: Blender as a tool for palaeontologists with a case study on extinct arachnids

    J. Palaeontol.

    (2014)
  • R.J. Garwood et al.

    High-fidelity X-ray microtomography reconstruction of siderite-hosted Carboniferous arachnids

    Biol. Lett.

    (2009)
  • S. Harzsch et al.

    Evolution of arthropod visual systems: development of the eyes and central visual pathways in the horseshoe crab Limulus polyphemus Linnaeus, 1758 (Chelicerata, Xiphosura)

    Dev. Dynam.

    (2006)
  • C. Haug

    The evolution of feeding within Euchelicerata: data from the fossil groups Eurypterida and Trigonotarbida illustrate possible evolutionary pathways

    PeerJ

    (2020)
  • C. Haug et al.

    The evolutionary history of body organisation in the lineage towards modern scorpions

    Bull. Geosci.

    (2019)
  • M.J. Henzey et al.

    The dynamic evolutionary history of pancrustacean eyes and opsins

    Integr. Comp. Biol.

    (2015)
  • D.T. Hoang et al.

    UFBoot2: improving the ultrafast bootstrap approximation

    Mol. Biol. Evol.

    (2018)
  • R.J. Howard et al.

    Exploring the evolution and terrestrialization of scorpions (Arachnida: Scorpiones) with rocks and clocks

    Org. Divers. Evol.

    (2019)
  • D. Huang et al.

    Origin of spiders and their spinning organs illuminated by mid-Cretaceous amber fossils

    Nat. Ecol. Evol.

    (2018)
  • J.R.S. Hunter

    Notes on the discovery of a fossil scorpion (Palaeophonus caledonicus) in the Silurian strata of Logan water

    Trans. Geol. Soc. Glasg.

    (1886)
  • A.J. Jeram

    Phylogeny, classification and evolution of Silurian and Devonian scorpions

  • F.M. Jones et al.

    Trigonotarbus johnsoni Pocock, 1911, revealed by X-ray computed tomography, with a cladistic analysis of the extinct trigonotarbid arachnids

    Zool. J. Linn. Soc.

    (2014)
  • C. Kamenz et al.

    Sperm carriers in Silurian sea scorpions

    Naturwissenschaften

    (2011)
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