Review Article
Arthropod phylogeny: An overview from the perspectives of morphology, molecular data and the fossil record

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Abstract

Monophyly of Arthropoda is emphatically supported from both morphological and molecular perspectives. Recent work finds Onychophora rather than Tardigrada to be the closest relatives of arthropods. The status of tardigrades as panarthropods (rather than cycloneuralians) is contentious from the perspective of phylogenomic data. A grade of Cambrian taxa in the arthropod stem group includes gilled lobopodians, dinocaridids (e.g., anomalocaridids), fuxianhuiids and canadaspidids that inform on character acquisition between Onychophora and the arthropod crown group. A sister group relationship between Crustacea (itself likely paraphyletic) and Hexapoda is retrieved by diverse kinds of molecular data and is well supported by neuroanatomy. This clade, Tetraconata, can be dated to the early Cambrian by crown group-type mandibles. The rival Atelocerata hypothesis (Myriapoda + Hexapoda) has no molecular support. The basal node in the arthropod crown group is embroiled in a controversy over whether myriapods unite with chelicerates (Paradoxopoda or Myriochelata) or with crustaceans and hexapods (Mandibulata). Both groups find some molecular and morphological support, though Mandibulata is presently the stronger morphological hypothesis. Either hypothesis forces an unsampled ghost lineage for Myriapoda from the Cambrian to the mid Silurian.

Introduction

Arthropods have been the dominant component of animal species diversity for all of the past 520 million years, since the main burst of the Cambrian radiation. The earliest arthropod body fossils are confidently dated to Stage 3 of the Cambrian (Fig. 1), though some records have been assigned to Stage 2 (Steiner et al., 1993, Steiner et al., 2005). The trace fossil record of Arthropoda is generally regarded as predating the body fossil record, with Monomorphichnus and Rusophycus traces that are widely endorsed as being arthropodan extending back into Stage 2, from strata traditionally assigned to the Tommotian (Budd and Jensen, 2000).

For the purpose of this review, major competing hypotheses for the fundamental groupings in the Arthropoda are introduced by their proper names. I see little point in presenting “the” morphological perspective and (or versus) “the” molecular perspective because morphologists have advocated hypotheses as different from each other as any of them are to any molecular result (morphologists have supported either Tetraconata or Atelocerata, Mandibulata or Schizoramia, etc.). Likewise there is no singular molecular tree for arthropods because different genes or different analyses have differed in the clades that they resolve. That said, certain recurring patterns can be recognised with different classes of evidence, e.g., molecular phylogenies are split between myriapods being most closely allied to chelicerates (Paradoxopoda/Myriochelata) or to hexapods and crustaceans (Mandibulata), but irrespective of what markers are employed, a hexapod–crustacean clade (Tetraconata) is emphatically favoured rather than a myriapod–hexapod clade (Atelocerata).

One region of the arthropod tree is the domain of a singular class of data, the resolution of the stem group. Fossils provide the only evidence for the sequence of branchings and character acquisition in the arthropod stem group. This field has advanced considerably in recent years, and a substantial degree of consensus has emerged with respect to such hypotheses as gilled lobopodians, anomalocaridids and other dinocaridids, and fuxianhuiids being positioned in the stem group of Arthropoda.

Arthropod phylogeny is sometimes presented as an almost hopeless puzzle wherein all possible competing hypotheses have support (“chaos” fide Bäcker et al., 2008, fig. 1). It is certainly the case that a great diversity of groupings has been advocated through the decades, and much of this diversity is seen even in contemporary work. However, it needs to be emphasised that the field of strongly supported competing theories has been winnowed down, and current debates focus on a few alternatives that each generally finds support from different kinds of evidence (Budd and Telford, 2009).

Section snippets

The sister group of Arthropoda: Onychophora or Tardigrada?

Arthropoda is here used in the sense of most English-language sources, that is, excluding Onychophora and thus corresponding to “Euarthropoda” in much European literature. Identifying the sister group of the arthropods has obvious importance for evaluating character polarity at the base of Arthropoda. Two competing theories are currently relevant to the arthropod sister group: either onychophorans or tardigrades are the closest relatives of arthropods. Both of these theories share a common

Arthropod monophyly: no longer a controversy

The popular mid-20th Century theory that arthropods were polyphyletic (Tiegs and Manton, 1958, Anderson, 1973, Schram, 1978) had its critics even in its heyday (e.g., Lauterbach, 1974). The fundamental failure of arthropod polyphyly was that its advocates never identified any real groups of organisms as the sister groups of the different arthropod branches. When imaginary worms are removed from trees depicting the ancestry of arthropod lineages (Fryer 1996, fig. 1), the branches converge on

Chelicerata, Myriapoda, Crustacea and Hexapoda: monophyly and challenges

The deep relationships of arthropods amount to the arrangement of chelicerates, myriapods, crustaceans and hexapods. Of these four groups, the monophyly of each has been questioned at some point, though in current literature only Crustacea finds widespread recognition as probably being non-monophyletic. Because evidence for and against monophyly is appraised in detail in the chapters on each of these groups, only a brief summary is given here.

Mandibulata

A clade of arthropods in which the post-tritocerebral appendage assumes the form of a jaw or mandible (Fig. 4A) has provided the traditional basis for uniting myriapods, crustaceans and hexapods as Mandibulata. The homology of the mandible has been defended on morphological (Bitsch, 2001, Edgecombe et al., 2003) as well as gene expression (Prpic and Tautz, 2003) grounds. Additional anatomical evidence for the monophyly of Mandibulata has been summarised by Wägele (1993) and Harzsch et al. (2005)

Stem group Arthropoda

Comparison of crown group arthropods and their extant sister group, Onychophora, is the morphological equivalent of a long branch problem, and it is not a surprise that the controversy over Mandibulata versus Paradoxopoda has been described as a rooting problem (Giribet et al., 2005, fig. 1). Given that no additional extant taxa can be added to the sample to try and break up the long branches that separate (crown group) arthropods and onychophorans, fossils have a unique opportunity to inform

Closing “open questions”

Throughout this review I have attempted to differentiate between hypotheses that have fallen by the wayside in the face of conflicting evidence and hypotheses that continue to merit serious attention. In my opinion, too many summaries of arthropod phylogeny have been too quick to treat all nodes of the tree as an “open question” because some class of data (sometimes a single character) may support a group and that result was published. Often it turns out that those data were few and flawed. A

Acknowledgements

I thank Graham Budd and Allison Daley for discussion and collaboration on the arthropod stem group, and the former for the opportunity to study Pambdelurion. Images were kindly provided by Allison Daley, Derek Briggs, Tom Harvey, Markus Koch, Carsten Müller, Stefan Richter, Nick Strausfeld and Carsten Wolff. Research on arthropod relationships has been supported by the “Assembling the Protostome Tree of Life” project (NSF grants 0334932 and 0531757). Suggestions from the journal's referees

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