Origins and Early Evolution of Arthropods - Edgecombe et al. (2014)

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FRONTIERS IN PALAEONTOLOGY
ORIGINS AND EARLY EVOLUTION OF ARTHROPODS
by GREGORY D. EDGECOMBE1* and DAVID A. LEGG2
1Department of Earth Sciences, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK; e-mail: g.edgecombe@nhm.ac.uk
2Oxford University Museum of Natural History, Parks Road, Oxford, OX1 3PW, UK; e-mail: david.legg@oum.ox.ac.uk
*Corresponding author
Typescript received 13 January 2014; accepted in revised form 4 February 2014
Abstract: Phylogenomics reconstructs an arthropod tree in
which a monophyletic Arthropoda splits into Pycnogon-
ida + Euchelicerata and Myriapoda + Pancrustacea. The
same chelicerate–mandibulate groups are retrieved with morpho-
logical data sets, including those encompassing most taxa known
from Palaeozoic Konservat-Lagerst€atten. With respect to the
interrelationships of the three extant clades of Panarthro-
poda, a sister group relationship between Onychophora and
Arthropoda is endorsed by transcriptomics and microRNAs,
although this hypothesis forces homoplasy in characters of
the segmental ganglia that are shared by tardigrades and
arthropods. Cambrian lobopodians, dinocaridids, bivalved
arthropods and fuxianhuiids document the successive
appearance of characteristic arthropod features in the stem
lineage of Euarthropoda (crown-group arthropods). Mol-
ecular dating suggests that arthropods had their origin and
initial diversification in the Ediacaran, but no convincing
palaeontological evidence for Panarthropoda is available until
the earliest Cambrian.
Key words: Arthropoda, phylogenetics, morphology, mol-
ecules, fossils.
ARTHROPOD molecular phylogenetics moved at a fast
pace through the 2000s, starting the decade with parsi-
mony analysis of eight genes and morphology being near
the limits of computational capacity (Giribet et al. 2001)
and ending with densely sampled likelihood-based esti-
mates derived from 62 genes (Regier et al. 2010) and the
first broad coverage of arthropod diversity at a phyloge-
nomic scale (Meusemann et al. 2010). Arthropod palaeon-
tology has nearly kept pace, with discoveries from
Cambrian Konservat-Lagerst€atten informing on the earli-
est stages of arthropod history and the transition from
nonarthropod Ecdysozoa to crown-group euarthropods.
This article aims to concentrate on data and debates about
deep arthropod divergences since decade-ending reviews
by Budd and Telford (2009) and Edgecombe (2010a).
Relationships between major arthropod groups: a molecular
scaffold
Nucleotide sequences and/or amino acids have been the
source of several novel hypotheses about arthropod rela-
tionships since the field exploded in the mid-1990s. The
hypothesis that insects are nested within a paraphyletic
Crustacea, although proposed by neuroanatomists in the
early twentieth century, is perhaps the flagship example
of molecular evidence reshaping our understanding of
arthropod phylogeny. Until about 2008, molecular trees
were mostly based on analyses of a few genes, typically
the small and large nuclear ribosomal subunits, selected
mitochondrial genes or whole mitochondrial genomes, or
a few nuclear protein-encoding genes (see Giribet and
Edgecombe (2012) for review). The field has shifted fun-
damentally in the past few years by either greatly expand-
ing the number of genes from traditional targeted Sanger
sequencing or by sequencing random clones (expressed
sequence tags or ESTs) derived from cDNA libraries,
allowing entire transcriptomes to be mined for vastly lar-
ger numbers of genes. The most substantial ‘traditional’
data set is the 62-gene/75 arthropod sample of Regier
et al. (2010), which has been reanalysed in several subse-
quent studies (Regier and Zwick 2011; Zwick et al. 2012;
Lee et al. 2013; Rota-Stabelli et al. 2013a; Wheat and
Wahlberg 2013). The most comprehensive transcriptomic
data sets are those of Meusemann et al. (2010), Andrew
(2011), Rota-Stabelli et al. (2011) and von Reumont et al.
(2012). Oakley et al. (2013) and Rota-Stabelli et al.
(2013a) provide compilations of ESTs, mitochondrial
protein-coding genes, nuclear ribosomal genes and the
nuclear protein-coding genes of Regier et al. (2010).
Based on repeated, well-supported groupings in these
most recent and most densely sampled analyses, the fol-
lowing can be taken as the ‘molecular scaffold’ for the
arthropod tree (Fig. 1):
1. Pycnogonids (Fig. 2A) are sister group of Euchelicerata
rather than being sister group of all other arthropods.
© The Palaeontological Association doi: 10.1111/pala.12105 457
[Palaeontology, Vol. 57, Part 3, 2014, pp. 457–468]
2. Within Euchelicerata, Xiphosura is sister group of
Arachnida, as in traditional morphological trees, but
arachnid relationships are poorly resolved apart
from strong support for monophyly of Tetrapulmo-
nata and its internal resolution.
3. Mandibulata (a group of arthropods with mandibles
as the main adult mouthpart) is better supported than
the rival Paradoxopoda or Myriochelata hypothesis,
which united myriapods with chelicerates rather than
with other mandibulates (insects and crustaceans)
(Regier et al. 2010; Rota-Stabelli et al. 2011).
4. Myriapoda is monophyletic, its two main clades
being Chilopoda and Progoneata.
5. Progoneata may include a Symphyla + Pauropoda
clade (= Edafopoda; Zwick et al. 2012) rather than
the morphologically favoured Dignatha (= Diplo-
poda + Pauropoda).
6. Pancrustacea/Tetraconata is a clade that nests Hexa-
poda within the traditional ‘Crustacea’.
7. Oligostraca (a clade including Ostracoda, Branchiura
(fish lice), Pentastomida (tongue worms) and proba-
bly Mystacocarida) is sister group of all other Pan-
crustacea, collectively named Altocrustacea.
8. Malacostraca, Thecostraca and Copepoda unite as a
clade named Multicrustacea but whether it resolves
as Malacostraca + Thecostraca (= Communostraca;
Regier et al. 2010) or as Thecostraca + Copepoda
(= Hexanauplia; Oakley et al. 2013) is unsettled.
9. Branchiopoda, Remipedia and Hexapoda unite in a
clade named Allotriocarida (Oakley et al. 2013),
which also includes Cephalocarida (variably resolved
as closest relatives of branchiopods or of remipedes).
10. The closest crustacean relatives of hexapods are
remipedes.
11. Hexapoda is monophyletic, but the status of Entog-
natha as a clade or a grade remains uncertain
(Dell’Ampio et al. 2014). EST-based analyses that
support monophyly of Entognatha have conflicted over
whether it divides into Protura + Diplura (= Non-
oculata; Meusemann et al. 2010; Andrew 2011) or the
standard morphological resolution of Protura +
Collembola (= Ellipura; von Reumont et al. 2012).
The sister group: Onychophora or Tardigrada?
Arthropods belong to a clade of moulting animals with
paired, segmental ventrolateral appendages. The member-
ship of Arthropoda and Onychophora within this putative
clade, named Panarthropoda by Nielsen (1995), is uncon-
troversial, but the third member, the Tardigrada, has been
rather less stable, especially in phylogenomic studies. An
attraction between tardigrades and nematodes was a
recurring theme of multilocus and transcriptomic analy-
ses, which resolved tardigrades with nematodes under
some analytical conditions and, conflictingly, grouped
them with panarthropods under alternative conditions (e.g.
Dunn et al. 2008; Meusemann et al. 2010). Reanalysis of
data sets that have generated the tardigrade–nematode
group by Campbell et al. (2011), coupled with an expanded
sampling of genes, showed that signal for that group
increases under conditions expected to exacerbate long-
branch attraction, whereas conditions designed to counter
this kind of systematicerror found increased support for
the alliance between tardigrades and other Panarthropoda.
The phylogenomic analysis of Campbell et al. (2011) was
congruent with the topology (Tardigrada (Onychophora +
Arthropoda)) and the discovery of unique microRNAs in
that study supported the same groupings.
Thus, from a molecular perspective, monophyly of
Panarthopoda and a sister group relationship between
onychophorans and arthropods are the best supported
hypotheses. Additional support for affinities between tar-
digrades and arthropods from shared characters of the
segmental ganglia (Mayer et al. 2013a), including an ante-
rior (parasegmental) shift in the position of the ganglia
relative to their corresponding leg pair and segmental sets
of immunoreactive neurons, provides renewed support
for Panarthropoda in that these characters are not shared
by nematodes. However, the absences of the same features
in Onychophora has been taken as evidence that tardi-
grades rather than onychophorans are the sister group of
Arthropoda (Mayer et al. 2013a). This renews the Tacto-
poda hypothesis (= Tardigrada + Arthropoda) originally
formalized by Budd (2001) based on appendage structure.
Although certain fossils from Cambrian Konservat-
Lagerst€atten have been allocated to the stem group of
Onychophora (e.g. Antennacanthopodia: Ou et al. 2011)
and cladistic analyses have grappled with the tardigrade–
onychophoran–arthropod three-taxon problem by coding
all well-known Cambrian lobopodians, the lobopodian
part of the tree has been unstable and fossil analyses have
shown considerable topological conflict (Dzik 2011; Liu
et al. 2011; Ma et al. 2013). The question of how tardi-
grades are allied to arthropods is more likely to be
resolved phylogenomically than palaeontologically.
F IG . 1 . Molecular phylogenetic framework for extant Arthropoda, summarizing clades repeatedly resolved in multilocus or phylo-
genomic analyses, with divergences calibrated by fossil taxa (based on data in Lee et al. 2013, Rota-Stabelli et al. 2013b). Ranges are
depicted as extending to the base of polytomies but may be shorter in particular resolutions. Dashed lines within Arachnida indicate
morphological groupings that are not strongly contradicted by available molecular data.
458 PALAEONTOLOGY , VOLUME 57
EDGECOMBE AND LEGG : ARTHROPOD EVOLUTION 459
Head segmentation and fossils
Controversy over how the head segments of extant ar-
thropods are aligned was largely dispelled in the late
1990s when the expression domains of Hox genes were
first applied to the problem. The traditional concept that
chelicerates had lost a deutocerebral segment and that the
chelicera was innervated by the tritocerebrum was over-
turned when the anterior expression domain of labial, the
anteriormost gene of the arthropod Hox cluster, was
found to align the chelicera with the first antenna of
mandibulates (Damen et al. 1998; Telford and Thomas
1998). This alignment of the head was subsequently
corroborated by correspondences in the developing
A
E
G H I J
F
B C D
F IG . 2 . Cephalic appendage morphology and segmental affiliations. A, chelifores of the pycnogonid (Chelicerata) Austropallene sp.;
B–C, segmental correspondence of the chelicerate and mandibulate brain and affiliated appendages; D, ventral cephalic view of the
centipede (Mandibulata: Myriapoda) Digitipes jangii; E, frontal appendages of Anomalocaris canadensis (ROM 51213); F, ‘short-great-
appendages’ of Yohoia tenuis (USNM 155621); G–H, anterior anatomy and cephalic organization of Fuxianhuia protensa (YKLP
15006); I–J, nervous system in head and anterior part of trunk of the megacheiran Alalcomenaeus sp. (YKLP 11075), coincidence signal
of EDXRF Fe and microCT. For head diagrams, nervous tissue is yellow, structures associated with the protocerebrum are light blue,
deutocerebral structures are red, tritocerebral structures are green, the mouth is the dark blue oval, and internal black lines indicate
neural connections. Abbreviations: AN, antenna; CH, chelifores; DN, deutocerebral neuropil; FA, frontal appendage; GA, ‘great append-
age’; NT, neural tissues; OF, oesophageal foramen; PN, protocerebral neuropil; SPA, specialized postantennal appendage; TN, tritocere-
bral neuropil. Institutional abbreviations: ROM, Royal Ontario Museum, Canada; USNM, National Museum of Natural History,
Smithsonian Institution, USA; YKLP, Yunnan Key Laboratory for Palaeobiology, China.
460 PALAEONTOLOGY , VOLUME 57
nervous systems of Limulus and crustaceans (Mittmann
and Scholtz 2003) and is now widely endorsed (see
Fig. 2A–D for Chelicerata and Mandibulata).
More controversial has been the segmental composition
of the brains of the nonarthropod Panarthropoda, the
Onychophora and Tardigrada, that is, how many seg-
ments comprise the brain and their homologies with the
tripartite brain of arthropods. The tardigrade brain is
argued to be composed of a single segment, correspond-
ing to the arthropod protocerebrum alone (Mayer et al.
2013b; Schulze and Schmidt-Rhaesa 2013), or to possibly
include as many as two additional neuromeres (Persson
et al. 2012). According to nervous system development,
the onychophoran brain is assigned just two segments,
corresponding to the arthropod proto- and deutocere-
brum (Mayer et al. 2010). Hox expression domains indi-
cate that the third head segment of onychophorans,
which bears the slime papilla, is segmentally equivalent to
the tritocerebrum of arthropods (Eriksson et al. 2010),
although the corresponding ganglia do not originate from
the central neuropils of the onychophoran brain (Mayer
et al. 2010). Eriksson et al. (2010) postulated that the
protocerebral antennae of onychophorans and the labrum
of arthropods are homologous on the basis of Hox gene
alignment, whereas Frase and Richter (2013) instead
homologized onychophoran antennae with the frontal fil-
aments of crustaceans.
Even greater controversy surrounds the segmental
alignment of head structures in many fossil arthropods
and those of extant taxa, a manifestation of the so-called
‘arthropod head problem’ (Budd 2002; Scholtz and Edge-
combe 2006). Much of the debate involves the interpreta-
tions of structures in (mostly) Cambrian fossils variably
described as frontal appendages (Fig. 2E) or great
appendages (Fig. 2F). Whether raptorial appendages in
such taxa as anomalocaridids and megacheirans (the latter
being the ‘short-great-appendage arthropods’) belong to
the same head segment and with which neuromere of the
brain they are associated is the crux of the problem. Very
recent literature considers these appendages to either be
(Haug et al. 2012) or not be (Legg and Vannier 2013)
segmentally equivalent. In the case of megacheirans, the
segmental affiliation of the great appendages ranges from
them being protocerebral (Budd 2002), deutocerebral
(Tanaka et al. 2013; Yang et al. 2013) or tritocerebral
(Legg and Vannier 2013).
The conventional basis for identifying the segmental
association of modified appendages in fossil arthropods
has been to use structural correspondence in appendage
morphology (e.g. the elbow joint and chelate tip of
megacheiran great appendages suggest homology with
chelicerae; Haug et al. 2012) and to integrate their relation-
ships to other appendages (i.e. an apparent association of
megacheiran great appendages and antennae in some taxa
suggests the former are tritocerebral/postcheliceral if the
antennae are deutocerebral as in extant arthropods; Legg
et al. 2012, Legg and Vannier 2013). Recently, a few studies
have identified neural tissue in Cambrian fossils that allows
putative neuromeres of the brain to be associated withappendages (Fig. 2G–J). The brain of Fuxianhuia protensa
from the Chengjiang biota has identifiable neural tracts to
the ocular lobes, antennae and postantennal appendages
that associate these segmental structures with the proto-,
deuto-and tritocerebrum, respectively (Fig. 2G, H; Ma
et al. 2012a). This evidence has assisted the interpretation
of specialized postantennal appendages in Fuxianhuia
(Budd 2008; Yang et al. 2013) that had alternatively been
viewed as gut diverticulae (Waloszek et al. 2005). Likewise,
Tanaka et al. (2013) described neural tissue in Alalcomen-
aeus sp. (Fig. 2I, J), a megacheiran (‘short-great-append-
age’ arthropod). Segmental alignment with extant
chelicerates was argued to favour deutocerebral affinities
for the ‘short-great-appendages’.
Phylogenetic analyses of large morphological data sets
The interrelationships of extant arthropods had been the
subject of various quantitative cladistic analyses that had
provided support for such clades as Mandibulata, Myria-
poda and Pancrustacea (Rota-Stabelli et al. 2011; Lee
et al. 2013), but these analyses either included a very
select group of fossil terminals or omitted fossils entirely.
Excluding or under-sampling fossil diversity does not per-
mit a test of whether phylogenetic relationships between
extant taxa are altered by the inclusion of fossils. In con-
trast, another set of cladistic analyses have more compre-
hensively sampled fossil taxa and their characters but
excluded extant arthropods and nonfossilized characters
(e.g. Stein et al. 2013). This, conversely, fails to test
whether the relationships of extant taxa might affect the
resolution of fossil taxa, and it excludes the majority of
data available for inferring arthropod phylogeny (e.g.
sperm ultrastructure, brain anatomy), apparently out of
belief in a ‘missing data problem’ (Edgecombe 2010b).
To rectify the very limited sampling of fossils in arthro-
pod morphological data sets (or the exclusion of extant
taxa from fossil matrices), an increasing number of fossil
terminals have been coded in matrices modified from
those used to infer the relationships of extant taxa, and
the character sample has also been vastly increased. Legg
et al. (2012) analysed 173 panarthropods (97 fossils/76
extant) for a sample of 580 characters (see Legg and Van-
nier 2013; Legg and Caron 2013 for addition of taxa to
this matrix), whereas Legg et al. (2013) coded 753 charac-
ters for 309 panarthropod terminals of which 198 were
extinct (see Siveter et al. 2014 for the addition of five
more fossil terminals).
EDGECOMBE AND LEGG : ARTHROPOD EVOLUTION 461
With or without fossils, these morphological analyses
support the union of mandibulate arthropods as a clade,
rather than supporting a myriapod–chelicerate group
(Paradoxopoda/Myriochelata). Fossils break up the long
branch at the base of the Pycnogonida and their inclusion
contributes to resolving pycnogonids as chelicerates rather
than as sister to all other arthropods (= Cormogonida),
as found in most molecular analyses (Fig. 1) and consis-
tent with chelifores/chelicerae being a synapomorphy.
Also congruent with molecular studies, fossils contribute
to the resolution of ‘Crustacea’ as a paraphyletic group
with Hexapoda nested within, whereas the same character
set without fossils yielded crustacean monophyly (Legg
et al. 2013). Morphological cladograms either with or with-
out fossils do not recover several of the major groups
retrieved in molecular studies reviewed above, that is, mor-
phology does not support a basal split of Pancrustacea into
Oligostraca and Altocrustacea, nor does it retrieve Multi-
crustacea or Allotriocarida. Instead malacostracan and en-
tomostracan ‘crustaceans’ are largely separate assemblages
(Fig. 3). This cannot be argued to be an especially strong
critique of the phylogenomic groupings because the rival
morphology-based groups have poor branch support and
show considerable topological instability.
Character acquisition in the arthropod stem group
A wealth of new discoveries from early Palaeozoic Kons-
ervat-Lagerst€atten, combined with the application of
large-scale phylogenetic analyses, has had considerable
impact on our understanding of the early stages of
arthropod evolution. In particular, characters thought
indicative of arthropod affinities have been shown to be
acquired sequentially along the arthropod stem (Fig. 4).
The lobopodians have traditionally been considered
stem-group representatives of the three extant panarthro-
pod lineages and are therefore of considerable importance
for tracing the evolution of key characteristics in the
arthropod stem lineage. Diania cactiformis, a lobopodian
from the Chengjiang biota, was originally interpreted as
possessing arthropodized appendages (Liu et al. 2011), a
F IG . 3 . Pancrustacean relationships based on morphological data (based on Legg et al. 2013). Cephalocarida is resolved in this topol-
ogy within the traditional Maxillopoda.
462 PALAEONTOLOGY , VOLUME 57
key characteristic of arthropods, prompting a proposal
that sclerotization of the trunk appendages occurred
before sclerotization of the body (arthrodization).
A phylogenetic analysis by Liu et al. (2011) resolved
Diania in the arthropod stem lineage amongst the dino-
caridids, a clade of panarthropods that includes taxa with
arthropodized cephalic appendages but lacking trunk
appendages. Subsequent analyses were unable to repro-
duce these results (Legg et al. 2011; Mounce and Wills
2011) and instead resolved Diania more stemward in the
lobopodian grade, and a study of new material of Diania
cast doubt on the interpretation of the trunk appendages
as arthropodized (Ma et al. 2013).
Extant arthropods possessed a diverse array of visual
systems which differ in their number of visual elements
and their relative position. Numerous studies strongly
support a common origin for rhabdomeric compound
eyes of arthropods based on the ultrastructure of extant
exemplars (e.g. Harzsch et al. 2007), but details of their
origins have been obscure. The eyes of the lobopodians
Hallucigenia fortis and Luolishania longicrurus have
been interpreted as having a multicomponent structure
formed of individual ocelli, prompting comparison with
the lateral eyes of arthropods (Ma et al. 2012b). Given
prior hypotheses of phylogenetic relatedness, this struc-
ture may represent the precursor of the compound eyes
found in arthropods and dinocaridids, although conflict-
ing evidence either allies some of these taxa with ony-
chophorans rather than arthropods (Caron et al. 2013,
in the case of hallucigeniids) or interprets the eyes of
Cambrian lobopodians as simple ocelli (Ou et al. 2012;
Schoenemann and Clarkson 2012). The elucidation of
F IG . 4 . The successive acquisition of key arthropod characteristics in the euarthropod stem lineage (based on Legg et al. 2012, 2013).
Numbers indicate key innovations in the euarthropod stem lineage: (1) compound eyes; (2) arthropodized cephalic limbs; (3) arthro-
podized trunk limbs with an endopod (a) and exopod (b); (4) arthrodization; (5) specialized cephalic appendages; (6) differentiation
of tergal exoskeleton into ventral sternites (a) and dorsal tergites (b) with paratergal folds (c); and (7) reduction in the number of
endopod podomeres (a) associated with the acquisition of a gnathobasic basipodite (b).
EDGECOMBE AND LEGG : ARTHROPOD EVOLUTION 463
the visual surface of anomalocaridids (Paterson et al.
2011) indicates that complex visual systems, in this case
highly adapted to a macrophagous predatory lifestyle,
evolved early in the arthropod stem, prior to the origin
of arthropodizedtrunk appendages and sclerotization of
the body.
A restudy of anomalocaridid taxa has contributed some
features that strengthen the case for arthropod affinities
(Daley et al. 2013; Daley and Edgecombe 2014). In partic-
ular, the lateral cephalic elements of Hurdia have been
compared to the bivalved carapace of Cambrian bivalved
arthropods (Legg et al. 2012; Legg and Vannier 2013), the
latter forming a paraphyletic grade of organization at the
base of Arthropoda (Legg et al. 2012; Legg and Vannier
2013; Legg and Caron 2013). Other putative similarities
between anomalocaridids and basal members of the bival-
ved arthropod grade include the possession of a weakly
sclerotized trunk and a posterior tagma composed of
multiple pairs of lateral flap-like processes (Legg et al.
2012). Legg and Vannier (2013) noted similarities in the
structure of the frontal appendages of anomalocaridids
(Fig. 2E) and the cosmopolitan Cambrian bivalved
arthropod Isoxys and concluded that in both cases their
frontal appendages originated from the protocerebral
somite and were therefore homologous with the antennae
of onychophorans. They further noted that specialized
raptorial appendages (‘short-great-appendages’) first
appeared in basal bivalved arthropods and on that basis
proposed nonhomology to the chelicerae of chelicerates.
As noted above, the phylogenetic position of ‘short-
great-appendage’ arthropods (megacheirans) and the seg-
mental homology of their eponymous appendages have
been points of contention in recent studies. Neural argu-
ments for a deutocerebral affinity for the ‘short-great-
appendages’ (Tanaka et al. 2013) are consistent with their
structural similarities to chelicerae (Haug et al. 2012); this
interpretation is depicted in Figure 2I. A number of phy-
logenetic analyses have resolved megacheirans as sister
taxon to Chelicerata (e.g. Edgecombe et al. 2011; Lams-
dell et al. 2013; Stein et al. 2013), but Legg (2013) sug-
gested that this was a rooting artefact. Analyses including
a more diverse assemblage of nonarthropod taxa have
tended to resolve megacheirans as the paraphyletic sister
taxon of Euarthropoda (Daley et al. 2009; K€uhl et al.
2009; Fig. 4), regardless of how the segmental affinities of
the ‘short-great-appendages’ were interpreted (compare
Legg 2013 and Legg et al. 2013 for deuto- and tritocere-
bral codings, respectively).
Fossils and divergence dates
Early attempts at molecular dating commonly calculated
that arthropods had a long unfossilized history in the
Neoproterozoic, and this has been maintained in some
more recent studies (Wheat and Wahlberg 2013).
Improved relaxed clock methods and sounder integration
of palaeontological constraints have for the most part
nullified the case for arthropod history extending as far
back as the Cryogenian, but even modern molecular
dates usually estimate the split of Arthropoda from its
sister group and the fundamental splits within the
arthropod crown group (e.g. Chelicerata–Mandibulata
divergence) as being Ediacaran (Rehm et al. 2011; Rota-
Stabelli et al. 2013b). Even this comparatively short ‘phy-
logenetic fuse’ in the Ediacaran predates fossil evidence
for arthropods. Despite attempts to shoehorn Ediacaran
fossils such as Spriggina, Parvancorina and Archaeaspinus
into the arthropod stem- or crown groups (e.g. Lin et al.
2006; Peterson et al. 2008), these organisms share no
compelling characters with Arthropoda, and Panarthro-
poda as a whole is unrepresented in the fossil record
until the first Rusophycus traces are found in the Fortu-
nian. The Cambrian fossil record presents a strong case
that lobopodians (rather than Ediacarans) represent a
morphological grade in the stem groups of the three
panarthropod lineages.
If the palaeontological case for arthropod origins and
diversification in the Cambrian rather than the Neoprotero-
zoic is accurate, recovery of arthropod body fossils refer-
able to such extant crustacean groups as Branchiopoda
and Copepoda in palynological samples from the late
early and late Cambrian (Harvey and Butterfield 2008;
Harvey et al. 2012; Harvey and Pedder 2013) signals an
explosive radiation of crustaceans, and implicitly other ar-
thropods, during the Cambrian. The identification of
these fossils as members of extant crustacean total groups
contributes to molecular and morphological clock esti-
mates of rates of evolution amongst early arthropods sev-
eral times faster than background levels regardless of how
deeply in the Ediacaran the origin of Arthropoda is
allowed to extend (Lee et al. 2013).
Open questions
A coherent phylogeny of arthropods is falling into place,
but some fundamental questions still remain unanswered.
Amongst those that are almost exclusively the domain of
palaeontology, the search for the stem lineages of two
great terrestrial radiations, the Hexapoda and the Myria-
poda, tops the list. The Tetraconata/Pancrustacea hypoth-
esis predicts independent origins of terrestrial characters
in these two lineages, so we are faced with clades that
likely originated in the Cambrian and diversified in the
late Cambrian (Myriapoda) or Early Ordovician (Hexa-
poda) (drawing upon molecular dates from Rota-Stabelli
et al. 2013b), yet no convincing fossils are known until
464 PALAEONTOLOGY , VOLUME 57
the mid-Silurian (Myriapoda) or Early Devonian (Hexa-
poda), and these fossils are members of the crown
groups. A search image for a stem-group myriapod in the
Cambrian or Ordovician has been developed (Edgecombe
2004), but to date, no body fossils fill the lengthy ghost
lineage predicted by phylogeny. The Miracrustacea
hypothesis, which posits a remipede sister group of hexa-
pods (Figs 1, 3), may aid in refining a search image for a
stem-group hexapod.
Morphological cladistic analyses of crustaceans have
not yet converged on stable, well-supported groups, and
conflict remains with respect to such basic as issues as
whether or not Entomostraca is mono-, para- or polyphy-
letic, and the relationships of taxa traditionally grouped
as Maxillopoda. As noted above, no morphological analy-
sis has retrieved some of the groups depicted in the
‘molecular scaffold’ (Fig. 1), such as Altocrustacea, Multi-
crustacea and Allotriocarida. Incorporating fossils into a
phylogenetic synthesis for Tetraconata faces the challenge
of integrating character data filtered through different
styles of preservation, that is, Burgess Shale-type compres-
sion fossils, small carbonaceous fossils and secondarily
phosphatized ‘Orsten’-style fossils (Edgecombe and Legg
2013). Although a rich fossil record of early crustaceans is
turning up in the palynological fossil record, the fragmen-
tary nature of this material complicates resolving its asso-
ciations and phylogenetic position, but, as indicated
above, confident determinations are of great utility for
dating divergences. Likewise, Orsten ‘crustaceans’ from
the Cambrian of Sweden (Haug et al. 2010a, b) and
China (Zhang et al. 2007, 2010) may represent a small
fraction of potential crustacean diversity and continue to
be subject to diverse phylogenetic interpretations in large
part based on how larval data are coded (Boxshall 2007;
Wolfe and Hegna 2013), but they shed light on crown-
group Tetraconata in the Cambrian, and key morphologi-
cal innovations in the stem lineage of Mandibulata, such
as the development of endites as trunk limb-like cephalic
appendages were modified into mouthparts (Waloszek
et al. 2007).
In the case of Chelicerata, molecular analyses lag
behind morphology. The intense effort directed at resolv-
ing crustacean and insect relationships withtranscripto-
mes has not yet been matched for chelicerates, and
published molecular trees in part depict weakly supported
groups that conflict with stronger morphological data.
For example, nuclear-coding genes provide weak support
for an assemblage called Pulmonata that groups scorpions
with Tetrapulmonata (Regier et al. 2010), whereas mor-
phology unites Scorpiones and Opiliones (Shultz 2007).
Monophyly (morphology) versus polyphyly (molecules)
of Acari is likewise an issue. The morphologically delim-
ited arachnid clades Stomothecata and Haplocnemata
depicted in Figure 1 cannot be regarded as strongly con-
tradicted by the available molecular data. Forthcoming
genomic data for Chelicerata such as a recently published
scorpion genome (Cao et al. 2013) should provide better
tests of morphological hypotheses.
Acknowledgements. We thank Drs Claudia Arango, Allison Daley
and Joachim Haug for images in Figure 2A, E and F, respect-
ively, and the referee and Editor for input.
Editor. Andrew Smith
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