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