Review ArticleGeological history and phylogeny of Chelicerata
Introduction
Chelicerata s.l. includes Arachnida, Xiphosura, the extinct Eurypterida and Chasmatapspidida, and – more controversially – Pycnogonida. More than 100 000 recent species have been described, and in megadiverse groups like mites and spiders this number continues to increase substantially year on year. Arachnids and their relatives are thus the second most diverse group of modern arthropods after the hexapods. Most chelicerates are terrestrial and generally fill the role of predators, feeding on other arthropods or occasionally small vertebrates. As a group, mites exhibit a broader ecological spectrum which includes ectoparasitism, detritivory and plant-feeding. Although presumably derived from aquatic ancestors, marine and fresh-water chelicerates are less common today and restricted to the sea spiders, horseshoe crabs, and a few secondarily aquatic spiders and mites (especially Hydracarina). It should be added that the mid to late palaeozoic Eurypterida was a substantial aquatic group at that time and may well have included the largest arthropods ever to have lived (Braddy et al., 2007).
Chelicerata has traditionally received only cursory treatment in palaeontological textbooks. Despite this neglect, fossils of arachnids and their relatives are actually more diverse and abundant than might be expected. Dunlop et al. (2008b) documented nearly 2000 currently valid fossil chelicerate species in the literature; ca. 1600 of them arachnids. Since this publication, Wunderlich (2008) has added about 100 more spider species. Much of this palaeodiversity is concentrated into localities yielding exceptional preservation (Table 1). There is also substantial bias in favour of particular groups – spiders especially – and it is not clear to what extent this reflects real diversity patterns from former eras or how much of this is collection bias or the result of intensive study by Wunderlich, 1986, Wunderlich, 1988, Wunderlich, 2004, Wunderlich, 2008 in particular, who created many taxa based on weak, non-cladistic evidence. The last comprehensive study documenting first and last geological occurrences of chelicerate taxa was Selden's (1993a) contribution to Fossil Record 2; together with the corresponding summary by Selden (1993b). Further reviews can be found in Selden and Dunlop, 1998, Dunlop and Selden, 2009, and references therein. Much of the basic pattern outlined in Selden, 1993a, Selden, 1993b remains valid, although important discoveries in the last few years have pushed back the oldest limits of some lineages quite substantially.
The principal value of the fossil record is in documenting minimum ages for cladogenesis (Table 2). For example scorpions go back nearly 430 Ma and further finds could potentially push the oldest dates back even further. Assuming that a given lineage must be at least as old as its sister-group, stratigraphical occurrences can be superimposed onto cladograms (Fig. 1) to predict the presence of groups whose fossil record is either sparse or absent. Among arachnids, this extrapolation through so-called range extension and ghost lineages has been applied most successfully to spiders (Penney et al., 2003).
The resulting evolutionary trees – combining cladograms with the fossil record – can be used to help calibrate (or even falsify) molecular clocks (Dunlop and Selden, 2009), and/or to constrain estimates of divergence times inferred from molecular markers (Giribet et al., 2009, Fig. 10 for opilionids). They also reveal how well the fossil record fits a given estimate of phylogeny. An extreme view would actually be to sacrifice parsimony in favour of a better stratigraphic fit; as advocated in stratocladistics (cf. Fisher, 2008; and references therein). Shultz (1994) critically discussed this controversial methodology as specifically applied to arachnids. Nevertheless, conflicts between a taxon's best supported position in a cladogram and its oldest stratigraphic record can and do exist. Scorpions are, at ca. 428 Ma, the oldest unequivocal arachnids. They resolve as basal arachnids in some hypotheses (Weygoldt and Paulus, 1979), but as more derived in others (Shultz, 1990, Shultz, 2007, Giribet et al., 2002). Discrepancies between geological history and phylogeny present us with specific challenges for our future understanding of arachnid evolution.
In general, the role of individual fossils in phylogenetic reconstruction has always been controversial. The situation for Chelicerata is no exception (see e.g. 4.8). Even the best preserved fossils can never reveal the full suite of morphological (and of course molecular) characters available from living specimens. That said, recent advances in imaging techniques are dramatically improving both the quantity and quality of information that can be retrieved. Chelicerate examples include virtual fossils reconstructed by grinding through the matrix (Orr et al., 2000, Siveter et al., 2004), X-ray computer tomography (micro-CT) (Henderickx et al., 2006, Penney et al., 2007, Garwood et al., 2009, Heetoff et al., 2009) and combining images at different focal planes within translucent material (Kamenz et al., 2008). It is to be hoped that such improvements in methodology will reduce the number of equivocal characters which make comparisons between fossils and living forms so challenging.
Most fossil chelicerates can be assigned to existing crown-group taxa or clearly-definable extinct (Palaeozoic) orders. There are, however, exceptions. Amongst sea spiders (Pycnogonida), horseshoe crabs (Xiphosura), scorpions (Scorpiones) and whip scorpions (Theyphonida) there are some very old fossils, noticeably different from living forms, which offer the potential to reconstruct stem-lineages and ground pattern character states for these groups. Furthermore, a handful of enigmatic taxa have proved difficult to place within the traditional orders, usually because they are incomplete. It should also be stressed that there are no clear examples of missing links in the arachnid fossil record – although the recently proposed Uraraneida of Selden et al. (2008a) probably comes closest – revealing transitions from one major clade to another, or that unequivocally resolve between competing higher-level phylogenetic hypotheses. Perhaps for this reason, historical attempts to reconstruct arachnid phylogeny usually paid scant attention to fossil groups, or simply excluded them entirely (Wheeler and Hayashi, 1998). More integrative studies (Shear et al., 1987, Selden et al., 1991, Giribet et al., 2002, Shultz, 2007) include extinct taxa among the terminals and our present understanding of arachnid geological history is summarized here in the hope of encouraging further work of this nature.
Section snippets
Methods
Fossil Chelicerata and their relatives were reviewed from the literature, together with hypotheses about their probable stem-lineage and evolutionary relationships. The sequence of taxa and clade names adopted here essentially follows the most recent and comprehensive estimate of phylogeny by Shultz (2007). As a caveat, some of these clades are better supported than others and specific areas of conflict and alternative hypotheses are noted where appropriate. A distinction is made between the
Arthropods resembling horseshoe crabs
Chelicerata s.l., or even Euchelicerata, does not have a clearly defined stem-lineage. There is no fossil which can unequivocally be accepted as a common ancestor of the group. Historically, chelicerates were often assumed to be related to – perhaps even derived from – the extinct trilobites (Raw, 1957, Lauterbach, 1983, Weygoldt, 1998). This concept was largely based on similarities between trilobites and (larval) horseshoe crabs, and has been formalised under clade names like Arachnata or
Chelicerata s.l. (Cambrian–Recent)
The textbook concept of Chelicerata groups together Pycnogonida and Euchelicerata, a clade supported primarily by the chelate chelifores of sea spiders and the chelicerae of euchelicerates; see Dunlop and Arango (2005) for a review. Recent debate has focused on whether sea spiders are indeed the sister-group of Euchelicerata, or of a clade named Cormogonida comprising all non-pycnogonid euarthropods. Edgecombe (2010) reviews these alternative scenarios in further detail. Significantly,
Acknowledgements
I thank Paul Selden and Greg Edgecombe for helpful comments, and those colleagues who provided images as detailed under the figure legends.
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