Current Biology

Review

The Phylogeny and Evolutionary History of Arthropods

Gonzalo Giribet1,* and Gregory D. Edgecombe2
1Museum of Comparative Zoology & Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge,

MA 02138, USA
2Department of Earth Sciences, The Natural History Museum, London SW7 5BD, UK

*Correspondence: ggiribet@g.harvard.edu
https://doi.org/10.1016/j.cub.2019.04.057

Arthropods are the most diverse animal phylum, and their phylogenetic relationships have been debated for
centuries. With the advent of molecular phylogenetics, arthropods were found to be monophyletic and
placed within a clade of molting animals, the ecdysozoans, with nematodes and six other phyla. Molecular
phylogenetics also provided a new framework for relationships between the major arthropod groups, such
as the clade Pancrustacea, which comprises insects and crustaceans. Phylogenomics based on second-
generation genomics and transcriptomics has further resolved puzzles such as the exact position of myria-
pods or the closest crustacean relatives of hexapods. It is now broadly recognized that extant arthropods are
split into chelicerates and mandibulates, and relationships within the two mandibulate clades (myriapods and
pancrustaceans) are stabilizing. Notably, the phylogeny of insects is now understood with considerable con-
fidence, whereas relationships among chelicerate orders remain poorly resolved. The evolutionary history of
arthropods is illuminated by a rich record of fossils, often with exquisite preservation, but current analyses
conflict over whether certain fossil groups are stem- or crown-group arthropods. Molecular time-trees cali-
brated with fossils estimate the origins of arthropods to be in the Ediacaran, while most other deep nodes
date to the Cambrian. The earliest stem-group arthropods were lobopodians, worm-like animals with annu-
lated appendages. Confidently placing some key extinct clades on the arthropod tree of life may require less
ambiguous interpretation of fossil structures and better integration of morphological data into the phylogeny.

Introduction candidates for the closest relatives of insects, and determining

Other than vertebrates, arthropods are perhaps the best-known
creatures on our planet and have attracted our attention in many
different ways. Arthropod-related folklore and representations
are popular in nearly all human cultures. They are a main source
of protein for many human populations, especially in coastal
areas, and it is now well established that most plants are polli-
nated by arthropods [1]. Research on arthropods has therefore
focused on diverse aspects of their biology, including fisheries,
aquaculture, apiculture and pollination biology, disease and
perhaps most prominently, genetics and evolutionary biology.
The fruit fly Drosophila melanogaster is one of the best-studied
animals, its genome having been sequenced before that of hu-
mans [2]. Since then, many arthropod genomes have been
sequenced but only a fraction of these are publicly available.
They total more than 420 species, representing 162 of about
3,000 arthropod families (as of May 2019 http://i5k.github.io/
arthropod_genomes_at_ncbi). Several initiatives, including the
5000 arthropod genomes initiative (i5K), continue to expand cur-
rent genome sampling to unprecedented levels [2,3].
In addition, a great deal of taxonomic research has been con-
ducted on arthropods, with vastly more species named and
described (ca. 1.02 million) than all remaining organisms on Earth
combined. This huge diversity, as well the breadth of anatomical
and functional disparity between and within major arthropod
lineages (Figure 1), has led to considerable interest in resolving
the arthropod tree of life. Fundamental evolutionary questions,
such as how and how often arthropods transitioned from water
to land or how pterygote insects evolved the ability to fly, are
centered on debates about phylogeny (e.g., choosing between
whether land-dwelling arachnids have a single origin).
The evolutionary implications of arthropod phylogeny have
been reviewed on multiple occasions [4–6], but these predate
the advent of transcriptomic and genomic data that have so
much refined our knowledge on relationships of chelicerates
[7,8], myriapods [9], ‘crustaceans’ and insects [10–12], as well
as arthropods as a whole [3,13]. Here, we take stock of
arthropod relationships in the light of the latest morphological,
molecular and paleontological evidence, and put these into an
evolutionary framework that becomes useful for those who study
other aspects of arthropod biology.
Arthropods and Other Animals
Not everyone agrees on what an ‘arthropod’ is, so we must pro-
vide some definitions. Arthropods are ecdysozoans, a clade of
molting protostomes that also includes such phyla as Nematoda
(roundworms), Nematomorpha (horsehair worms) and Priapulida
(penis worms) [14]. Within Ecdysozoa, a likely clade named ‘Pan-
arthropoda’ includes animals with paired segmental ventrolat-
eral appendages. Panarthropods comprises three clades that
many authors classify as phyla, namely Tardigrada (water bears),
Onychophora (velvet worms), and Arthropoda, also called by
some ‘Euarthropoda’ [15]. In all panarthropods, the body is
divided at least into a head and a trunk (these structurally and
functionally distinct batches of segments are known as tagmata),
but more tagmata are common, such as in insects (and other
hexapods) which have a head, thorax and abdomen.
The discussion about whether Arthropoda or Euarthropoda is
more or less appropriate for the sister group of Onychophora

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Current Biology
Review
gets cumbersome and is rooted in the 19th century, but these
names may conflict with current phylogenetic relationships and
phylogenetic thinking. In addition, the name Arthropoda refers
to the process of ‘arthropodization’, which distinguishes be-
tween animals with soft cuticles and those with appendages
that have sclerotized articles separated by a ring of unsclerotized
cuticle (known as ‘arthrodial membrane’). The sclerotized arti-
cles are articulated by hinges, condyles or pivot joints, and
such appendages have specific extrinsic and intrinsic muscula-
ture connecting the articles. All extant arthropods adhere to this
definition (except in a few cases of extreme parasitism), but
neither tardigrades nor onychophorans have undergone this pro-
cess. Arthropodization therefore occurred, evolutionarily, along
the stem lineage leading to extant arthropods, and fossils posi-
tioned along this stem show different degrees of arthropodiza-
tion. These are the many lineages of so-called stem-group ar-
thropods [16]. These fossil taxa, outlined below, are thus
integral to our understanding of arthropod evolution. From the
perspective of extant organisms, phylogenomic data position
onychophorans as the sister group of arthropods, their next
closest relative probably being tardigrades [14]. The latter posi-
tion is complicated by a persistent attraction of tardigrades to
nematodes and nematomorphs in molecular datasets, thus con-
tradicting the monophyly of panarthropods. However, in addition
to sharing segmental appendages, the three panarthropod phyla
share expression of the segment polarity gene engrailed at the
posterior boundary of developing segments [17], have a dorsal
ganglionar brain [18], and tardigrades and arthropods share
segmental ganglia in the ventral nerve cord with segmentally-
repeated sets of serotonin-like immunoreactive neurons [19]. A
novel microRNA has also been suggested to be a shared derived
character of panarthropods [20].
Therefore, even though our understanding of interrelation-
ships among the ecdysozoan phyla continues to be refined,
arthropods are probably related to tardigrades and onychopho-
rans, from which they are differentiated by having undergone
a total process of arthropodization.
Fossils and the Deepest Branches of the Arthropod Tree
The earliest evidence of arthropods comes from trace fossils,
resting traces assigned to the ichnogenus Rusophycus and loco-
motory traces assigned to Diplichnites from the earliest
Cambrian [16]. In sections in Newfoundland, where the global
standard for the Ediacaran–Cambrian boundary is defined, this
early arthropod behavior is likely to date to within a few million
years of the base of the Cambrian. Arthropod body fossils,
including the first trilobites, appear about 521 million years ago
(mya) and soon after (by 518 mya, the age of the Chengjiang
biota in China) are supplemented by diverse taxa in the oldest
Burgess Shale-type biota.
Irrespective of whether arthropods are more closely related to
onychophorans or to tardigrades, a recurring pattern in recent
phylogenetic analyses is that the deepest branch in the
arthropod stem-group is represented by large-bodied lobopo-
dians. ‘Lobopodians’ correspond to an evolutionary grade that
includes fossils in the stem groups of all three panarthropod
phyla, which have paired appendages in the form of annulated
lobopods [21]. The early Cambrian Megadictyon haikouensis
and Jianshanopodia decora exemplify these earliest arthropods,
which have an annulated trunk with a homonomous series of
lobopods. Key apomorphies shared with other stem-group ar-
thropods are an enlarged, annulated pair of frontal appendages
(thought to be innervated by the protocerebrum [22,23]) bearing
spines along their inner margin, and large, segmentally arranged
midgut diverticulae with a distinctive network of canals [24].
These characters are shared by the early Cambrian Pambdelu-
rion whittingtoni from Greenland [24,25], and together with large
body size indicate that early arthropods where macrophagous
and carnivorous. Pambdelurion and the co-occurring Kerygma-
chela kierkegaardi [23] have the body organized as a set of over-
lapping segmental flaps rather than a tubular worm-like trunk as
in the earliest lobopodian arthropods.
Some Cambrian clades with wide geographic distributions are
identified in many phylogenetic analyses as branching off after
the split of the lobopodians from the other stem-group arthro-
pods. This applies to radiodonts and to isoxyids [26]. Radiodonts
[27] — exemplified by the famous Anomalocaris (Figure 2E) —
are currently known from more than 25 species ranging from
the early Cambrian to at least the Early Ordovician [28], and
probably the Early Devonian if Schinderhannes bartelsi is a mem-
ber [29]. Unlike lobopodians, they possess additional arthropod
synapomorphies, notably a pair of large compound eyes [30] and
an arthropodized frontal appendage with strongly sclerotized ar-
ticles separated by softer membranous areas, with condyles on
the dorsal side of the articulations. While radiodonts are arthro-
podized they are not ‘arthrodized’ — their dorsal or ventral
cuticle is not sclerotized in the form of tergites and sternites,
respectively, a character that is apomorphic for a less inclusive
clade of stem- and crown-group arthropods. Fossils thus
uniquely reveal that arthropodization and compound eyes pre-
ceded arthrodization.
Currently, there are major discrepancies about how several
well-known Cambrian groups are placed in the arthropod tree
(Figure 2). This is most acute for the fuxianhuiids and for bivalved
arthropods collectively grouped as Hymenocarina [31]. Fuxian-
huiids (Figure 2G) are an early Cambrian group presently
known from eight species from Konservat-Lagersta €tten in South
China [32]. Hymenocarines (Figure 2F) include iconic Burgess
Shale taxa, such as Waptia fieldensis, Canadaspis spp., Odaraia
alata and the recently described Tokummia katalepsis [31].
Phylogenetic analyses had recovered both fuxianhuiids and hy-
menocarines as branching off in the arthropod stem-group
[33], particularly influenced by the interpretation of the head being
composed of few segments in both groups (Figure 2B). In striking
contrast, both have alternatively been placed in the arthropod
crown group, indeed within the stem (fuxianhuiids) or crown
group (hymenocarines) of the clade of jawed arthropods, the
Mandibulata (Figure 2C) [34]. These different placements
reflect different interpretations of cephalic structures — such as
whether or not fuxianhuiids have mandibles or whether the struc-
ture in question is part of the hypostome [35] — but also new dis-
coveries. In the case of Tokummia, material from the Marble
Canyon site of the Burgess Shale provides credible evidence
for additional head segments, including the differentiation of the
mouthparts as mandibles and maxillae. This discovery prompted
the reinterpretation of mandibles in Branchiocaris pretiosa [31].
Megacheirans, popularly known as ‘great appendage arthro-
pods’, present another key controversy in early arthropod
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A B C Figure 1. Representatives of major

arthropod extant lineages.
(A) Ventral view of Colossendeis sp. (Pycnogo-
nida); (B) Odiellus pictus (Arachnida, Opiliones);
(C) Gymnobisium inukshuk (Arachnida, Pseudo-
scorpiones); (D) Cryptocellus iaci (Arachnida,
Ricinulei); (E) Eukoenenia sp. (Arachnida, Palpi-
gradi); (F) Parascutigera latericia (Myriapoda,
Chilopoda, Scutigeromorpha); (G) Eudigraphis
taiwaniensis (Myriapoda, Diplopoda, Polyxenida);
D (H) Pauropus sp. (Myriapoda, Pauropoda); (I)
Hanseniella sp. (Myriapoda, Symphyla), (J) Light-
iella incisa (Cephalocarida); (K) Xibalbanus tulu-
mensis (Remipedia); (L) Holacanthella duospinosa
(Hexapoda, Collembola); (M) Podocampa fragi-
F loides (Hexapoda, Diplura, Campodeina); (N)
J Japyx sp. (Hexapoda, Diplura, Japygina). Photos:
(K, N) courtesy of Simon Richards and Jill Yager,
respectively; all other photos by the authors.

whether they are stem-group arthropods

G
[31], stem-group chelicerates [33,34] or
stem-group mandibulates [41]. Trilobites
include some 20,000 species with diag-
H nostic characters of their calcitic exoskel-
eton, but they are united with numerous
K ‘trilobitomorph’ lineages that lack cutic-
ular biomineralization (Figure 2I). All
these artiopodans exhibit appendicular
tagmosis involving a flagelliform antenna
I followed by morphologically similar bira-
mous head and trunk appendages [42].
For a long time, artiopodans had been al-
L lied with chelicerates under the Arachno-
morpha hypothesis, based on characters
M N such as trilobation (the dorsal exoskel-
eton having a raised axial region between
lateral pleural fields) and exopods that
bear a broad field of lamellar setae. This
is consistent with some recent phyloge-
netic analyses (Figure 2B,C), but is con-
tradicted by others [31,41].
In summary, although some early
branches of the arthropod stem-group
evolution. Best known from the genus Leanchoilia (Figure 2H) are subject to broad consensus, current parsimony and Bayesian
and species in most Cambrian Burgess Shale-type biotas [36], analyses of morphological datasets present discordant pictures
these arthropods share a distinctive anterior appendage in which of whether several Cambrian clades are inside or outside the
an elbow joint separates a basal peduncle from a few distal arti- crown-group radiation of arthropods. Resolving these differences
cles that extend as long spines and, in some genera, bear a will require unambiguous interpretations of the most contentious
terminal flagellum. The elbow joint and fixed and movable fingers homologies, such as mandibles and an intercalary segment,
between the terminal articles have been cited as evidence for something that may require even more exquisitely preserved fos-
homology with chelicerae (the diagnostic first appendage pair sils than those currently available for study, but also employment
of chelicerates), and these characters as well as fossilized neural of novel techniques for the analysis of fossil morphology. For
structures have thus been used to assign megacheirans to the example, computed microtomography has been powerful for ex-
chelicerate stem-group [37,38]. This relationship to chelicerates tracting three-dimensional detail in Burgess Shale-type compres-
has also been found in some quantitative phylogenetic analyses sion fossils. Microtomographic study of the early Cambrian
[39], but they have been placed in alternative positions in other arthropod Ercaicunia multinodosa [43] elucidated the presence
analyses, including as stem-group arthropods [33,40] or stem- of tritocerebral antennae rather than a limbless intercalary
group mandibulates (Figure 2B,C) [34]. segment as had been proposed for allied hymenocarines [31].
The well-known trilobites and related Paleozoic taxa (grouped The new finding strengthens the positioning of these bivalved
with them as Artiopoda) are likewise embroiled in debate over arthropods as total-group pancrustaceans (Figure 2A,C) rather

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Figure 2. Fossils and arthropod evolution.
D E F
Alternative topologies highlighting key fossils for
understanding evolution of the main extant
arthropod lineages (in bold) and the arthropod
stem group. (A) Based on [31]; (B) based on [33]; (C)
based on [34]. Fossil exemplars of major clades as
follows: (D) Isoxys acutangulus (Isoxyida); (E)
A Anomalocaris saron (Radiodonta); (F) Perspicaris
Giant lobopodians
dictynna (Hymenocarina); (G) Fuxianhuia protensa
(Fuxianhuiida); (H) Leanchoilia superlata (Mega-
Onychophora
cheira); (I) Misszhouia longicaudata (Artiopoda); (J)
Tardigrada Apankura machu (Euthycarcinoidea). Images
Radiodonta †
courtesy of Allison Daley (E,F), Diego Garcı́a-
Bellido (D,H), Xiaoya Ma (G,I) and Emilio Vaccari (J).
Isoxyida † H Line drawings based on [33,80].
Megacheira †
G
Artiopoda †

Chelicerata

Fuxianhuiida † Mandibulates are named for the pres-

Euthycarcinoidea † ence of the eponymous biting append-
Hymenocarina † ages, while their homolog to the chelate
Myriapoda appendages of chelicerates is a pair of
Pancrustacea sensory appendages (antennae). Some
B I J mandibulates have a second pair of
Tardigrada C Giant lobopodians antennae in the segment immediately
Onychophora Onychophora
Giant lobopodians Tardigrada posterior, the tritocerebral segment. The
Radiodonta † Radiodonta †
Isoxyida † Isoxyida † mandibles of mandibulates are thus
Hymenocarina † Artiopoda †
Fuxianhuiida † Chelicerata serially homologous to the first pair
Megacheira † Megacheira †
Artiopoda † Fuxianhuiida †
of walking legs in chelicerates; this
Euthycarcinoidea †
Chelicerata
Myriapoda Myriapoda
segmental alignment of the head across
Pancrustacea Hymenocarina † the arthropods is supported both by
Euthycarcinoidea † Pancrustacea

than in the arthropod stem-group, and removes an implausible
evolutionary sequence in which antennae were forced to reap-
pear after an earlier loss.
Relationships among Major Lineages of Extant
Arthropods
Molecular phylogenetics emphatically ended any debate about
whether arthropods are a monophyletic group — rejecting the
idea of multiple origins of arthropods (polyphyly) championed
by some functional morphologists and developmental biolo-
gists [44]. Extant arthropods are divided into two large mono-
phyletic groups (Figure 3): Chelicerata (sea spiders, horseshoe
crabs, spiders, scorpions and their relatives) and Mandibulata
(myriapods, insects and many lineages of ‘crustaceans’). The
divergence between these clades is consistently dated to the
Precambrian with molecular techniques [11,45], usually to
the Ediacaran Period, although no body or trace fossil evidence
for arthropods occurs in sediments older than the earliest
Cambrian [16]. Chelicerates include numerous extinct and
extant lineages of arthropods and are characterized by a pair
of deutocerebral appendages (innervated by the second
segment of a tripartite brain) transformed into a generally
chelate (pincer-like) feeding structure formed by just two or
three discrete articles, called chelicerae (in euchelicerates) or
chelifores (in the sea spiders, pycnogonids). Some of the
best-known chelicerates, the members of the arachnid order
Araneae (spiders), do not have chelate chelicerae, but rather
they are more like a jackknife.
Current Biology
neuroanatomy and by correspondences
in the spatial expression of Hox genes
[22]. The monophyly of mandibulates
and sometimes that of chelicerates (with regards to the pycno-
gonids), had been disputed throughout the history of arthropod
phylogenetics, but both clades are now well supported based
on genomic data. A debate over Mandibulata versus Myrioche-
lata/Paradoxopoda (a grouping of myriapods and chelicerates
that recurred in early molecular phylogenies) has been high-
lighted in past reviews [4,46] or studies that presented the
case for systematic error [47]. This question has lost relevance
in the present decade as more data consistently supported Man-
dibulata.
Mandibulata are now clearly understood as being composed
of two main clades, Myriapoda and Pancrustacea. The latter,
also called Tetraconata (for the four cone cells in the crystalline
cones of the ommatidia), includes multiple lineages of crusta-
ceans (a term we use in an informal sense), one of which, remi-
pedes, constitutes the likely sister group of hexapods — the
clade that includes the insects [11]. Insects are thus just a sub-
set (albeit a phenomenally diverse one!) of hexapods and of
pancrustaceans. If one is to maintain as many traditional
groups as possible, it is easiest to say that arthropods are
divided into chelicerates, myriapods and pancrustaceans; it is
not acceptable anymore to say that they are divided into
chelicerates, myriapods, crustaceans and insects, because
crustaceans are paraphyletic and insects are just a subset of
Hexapoda. The alternative would be to divide pancrustaceans
into oligostracans, multicrustaceans, cephalocarids, branchio-
pods, remipedes and hexapods, and use other clade names
proposed over the past decade based on molecular trees,

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Pycnogonida
Figure 3. Summary chronogram of the
major arthropod lineages.
Xiphosura
Topology is largely based on phylogenomic ana-
Opiliones
lyses [9–11]; divergence dates mainly based on
Ricinulei [9,10,111,112]. Line drawings based on
Palpigradi [33,80,113,114]; Mystacocarida line drawing by

CHELICERATA
Acariformes Triton - Own work, CC BY-SA 4.0, https://

EUCHELICERATA
Parasitiformes commons.wikimedia.org/w/index.php?
Solifugae curid=69989974.
Pseudoscorpiones
Scorpiones

ARACHNOPULMONATA
TETRAPULMONATA
Araneae
Amblypygi
instance, some recent genomic data sug-
Thelyphonida

Chilopoda
gest a sister-group relationship between
horseshoe crabs and ricinuleids (also

MYRIAPODA
Symphyla

PROGONEATA
known as hooded tick spiders;

DIGNATHA
Pauropoda
Diplopoda Figure 1D) [8]. This relationship is not
Ostracoda
yet explained anatomically or genomi-

OLIGOSTRACA
Branchiura
Mystacocarida
cally and would mean that xiphosurans

MANDIBULATA
are secondarily marine, necessitating

MULTICRUSTACEA
Malacostraca
Copepoda some surprising character reversals

PANCRUSTACEA
Thecostraca (e.g., reacquisition of compound eyes
Cephalocarida

ALTOCRUSTACEA
and flagellate sperm), or that arachnids
Branchiopoda
Remipedia
became terrestrial independently multi-

ALLOTRIOCARIDA
Protura ple times, as in the case of crustaceans.
LABIOCARIDA
In the context of xiphosurans potentially
HEXAPODA

Ediacaran Cambrian Ordovician Silurian Devonian Carboniferous
550 500 450 400 350
such as Labiocarida, Allotriocarida and Altocrustacea. As this is
only likely to resonate with a few hardcore arthropod systema-
tists, we attempt to provide here a succinct summary of these
relationships (Figure 3) so they can be easily understood by
other zoologists.
Chelicerate Relationships
Chelicerate diversity is dominated by two mega-diverse groups
traditionally classified as orders: Araneae (spiders), with some
45,000 living species and Acari (mites and ticks), with ca.
50,000 species — although the monophyly of Acari is widely
disputed (but see [48]). Other familiar groups include scorpions
and daddy-long-legs (Opiliones). Chelicerate bodies are divided
into two main regions, called the ‘prosoma’ and ‘opisthosoma’,
the former bearing the feeding appendages (chelicerae), a pair
of sensory ‘legs’ called ‘palps’ or ‘pedipalps’, which are used
for sperm transfer in male spiders, and four pairs of walking
legs. Chelicerates are best known for their venom (in spiders
and scorpions, and also pseudoscorpions or ‘false scorpions’;
Figure 1C) and their silk (in spiders, but also present in pseudo-
scorpions) [49].
Extant chelicerates have been traditionally divided into Pycno-
gonida (Figure 1A) and Euchelicerata, the latter split into the
marine Xiphosura (horseshoe crabs) and the largely terrestrial
Arachnida. This is consistent with a single shift from marine to
terrestrial habitats in a common ancestor of all extant arachnids,
although some mites have become secondarily aquatic,
spending their entire lives in water, unlike some semi-aquatic
spiders or palpigrades. However, the monophyly of arachnids
has been repeatedly challenged with molecular characters, for
Collembola
Diplura being secondarily marine, it may be
Insecta
meaningful that they lay eggs ashore, a
rarity among ancestrally marine animals.
300
Current Biology
Although arachnid monophyly is recov-
ered in some other genomic-scale ana-
lyses [48], our understanding of arachnid
relationships remains highly deficient, despite many decades of
detailed anatomical studies and vast amounts of molecular data
[49,50]. Indeed, other than the deep split between Pycnogonida
and Euchelicerata, and the resolution of the recently recognized
clade Arachnopulmonata (scorpions as sister group to arachnids
with two pairs of book lungs, or tetrapulmonates; i.e., Araneae,
Amblypygi, Uropygi and Schizomida [7]), many options
remain for the relationships between major groups, including
the diverse clades of mites and ticks, Pseudoscorpiones
(Figure 1C), Opiliones (Figure 1B), Solifugae and Palpigradi
(Figure 1E). One of the possible reasons for the inconsistencies
between morphology and molecules could be the large degree
of convergence in many arachnid groups that have become mini-
aturized [51], but this does not explain the lack of congruence
among the many published molecular data sets. Extinction of
many early lineages [52] in this phylogenetically old and diverse
group could add to the lack of consistent phylogenetic resolu-
tion. A roadmap to resolve these relationships is not easy to
draw, but current approaches focus on testing the specific posi-
tion of individual orders with their putative sister groups [8]
instead of approaches focusing on larger taxonomic sampling,
or on the study of broad-scale genomic changes and whole
genome duplications, including the specific duplication of ho-
meobox gene clusters [53,54]. The availability of more chelicer-
ate genomes should help with these questions, most importantly
trying to tease apart those chelicerates with the whole genome
duplication specific to arachnopulmonates from the rest.
The traditional hypothesis that scorpions are the sister group
of all arachnids [55] has been supplanted in recent decades by

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a hypothesis, also based on morphology, in which scorpions’
closest relatives are harvestmen (Opiliones). This putative clade
was named Stomothecata based on the elaboration of the pedi-
palp and first-leg endites, the preoral chamber described as a
stomotheca [56]. While the sister group of harvestmen remains
contentious from the perspective of molecular data, monophyly
of Stomothecata has been strongly contradicted by numerous
lines of evidence. Morphological characters from the book lungs
and hemolymph vascular system are now recognized to group
scorpions with tetrapulmonates [57], even though such charac-
ters had been previously considered striking convergences [58]
or shared primitive characters of the last arachnid common
ancestor. Resolution among the five extant arachnopulmonate
orders is now well established [7,8], but the addition of the
extinct Uraraneida has added some ambiguity [59,60]. In addi-
tion, it is unclear whether pseudoscorpions and the putative
Ricinulei–Xiphosura clade are closely related to arachnopulmo-
nates according to very specific developmental and genomic
similarities among some of these taxa.
The fossil record of chelicerates extends to the early Cambrian,
about 514 mya, and is exemplified by Wisangocaris barbarahar-
dyae from South Australia and the closely allied Sanctacaris un-
cata from the Burgess Shale. In phylogenetic analyses they are
more closely allied to euchelicerates than are pycnogonids [61].
Many Paleozoic chelicerates have a superficially horseshoe
crab-like appearance and were grouped as Synziphosurina,
often regarded as stem-group xiphosurans (true horseshoe
crabs). Synziphosurines are now instead considered to be a para-
phyletic assemblage, an evolutionary grade at the base of all
crown-group euchelicerates [62]. The traditional hypothesis
that arachnids are a monophyletic terrestrial radiation generally
infers that horseshoe crabs and sea scorpions (the Ordovician–
Permian eurypterids) are a primitively aquatic grade, with euryp-
terids being more closely allied to arachnids. Eurypterids (but not
horseshoe crabs) and arachnids share sclerophores, structures
involved in the production of spermatophores [63], signaling the
origin of the usual arachnid sperm-transfer mechanism in the
transitional environments inhabited by eurypterids.
In summary, novel data have resolved important clades of the
chelicerate tree, especially among Arachnopulmonata, and sur-
prising but consistent results place Xiphosura within Arachnida.
However, numerous arachnid orders remain phylogenetically
unstable.
Myriapod Relationships
Myriapods are divided into four major groups (usually ranked as
classes or subclasses): Chilopoda (centipedes), Diplopoda (milli-
pedes), Symphyla and Pauropoda. Centipedes are a well-known
predatory group of biomedical interest due to their potent venoms
[64], produced by a gland housed in a modified first pair of trunk
legs, and have one pair of legs per segment. Millipedes, with two
pairs of legs in most segments (called diplosegments), play an
important role in decomposing vegetal matter and cycling nutri-
ents back into the soil. Symphylans (Figure 1I) and pauropods
(Figure 1H) are blind soil arthropods with 12 and 8–11 pairs of
walking legs, respectively, and include relatively few species (ca.
200 and 850, respectively). Centipedes and millipedes comprise
ca. 3,500 and more than 12,000 species, respectively.
The phylogenetic status of myriapods was subject to more
than a century of debate, different authors endorsing either
monophyly or polyphyly. Some advocated paraphyly in the
context of myriapods being a grade in a grouping that contained
hexapods (collectively Atelocerata or Tracheata) [65]. Apart from
a few morphologists, this idea has been discarded in light of the
strong evidence for Pancrustacea, and myriapod monophyly is
found in nearly all molecular phylogenetic studies [9]. Myriapod
genomics, however, remains in its infancy — only the genomes
of the centipede Strigamia maritima [66] and the millipede Trigo-
niulus corallinus [67] are currently available.
Extant myriapods, despite often being associated with humid
environments, are strictly terrestrial and breathe through
tracheae. This predicts a terrestrial common ancestor, but the
marine roots of this lineage remain unclear. Because fossils as
old as 518 mya can convincingly be identified as crown-group
pancrustaceans [68], their myriapod sister group should likewise
date to the Cambrian, and molecular dating predicts a Cambrian
divergence at the base of myriapods [9,45]. Still, stem-group
myriapod fossils have not been found, and even the earliest po-
tential myriapod trackways are from the Late Ordovician and are
likely of subaqueous origin rather than terrestrial [69]. Among
candidates for marine stem-group myriapods, euthycarcinoids,
a clade that ranges from the late Cambrian (Figure 2J) to the
Middle Triassic, have emerged as the most plausible, and are
found in that position in recent Bayesian trees (Figure 2C) [34].
Admittedly, previous authors had considered some sort of
affinity to myriapods, but in the context of outdated phylogenetic
frameworks, such an ‘‘ancestral uniramian, or proto-antennate,
marine stock’’ [70] or as an ‘atelocerate’ relative [71], referring
to old ideas allying myriapods with onychophorans and insects
in ‘Uniramia’ or myriapods and insects as ‘Atelocerata’ or its syn-
onyms ‘Antennata’ and ‘Tracheata’.
The relationships between the four main groups of myriapods
have been a matter of debate and have been portrayed as a major
conflict between molecular and morphological phylogeny.
Morphology and development have traditionally supported a sis-
ter group relationship between millipedes and pauropods (a clade
named Dignatha for sharing only two pairs of gnathal append-
ages, the second maxillary segment being limbless), and have
also suggested symphylans being closely related to the
diplopod–pauropod group. These three groups together consti-
tute Progoneata (named for an anterior gonopore), with centi-
pedes as their sister group. In contrast, several molecular
datasets contradicted the clade Dignatha, in favor of a
symphylan–pauropod group named Edafopoda [72–75]. This
grouping had no evident morphological support apart from sym-
phylans and pauropods being blind (a condition also found in
many centipedes, including all geophilomorphs, and in polydes-
mid millipedes). However, densely sampled phylogenomic
analyses, including the first pauropod transcriptome, recently
recovered Dignatha with strong support, and showed that out-
group choice is critical for the inference of myriapod interrelation-
ships [9].
In summary, a lengthy debate over myriapod monophyly is
effectively settled, and a morphologically coherent set of internal
relationships is supported by current genomic-scale datasets
[76,77].
Pancrustacean Relationships and the Origin of Insects
Pancrustaceans include not only some of the most diverse clades
of arthropods, but also a great disparity in body plans, with
Current Biology 29, R592–R602, June 17, 2019 R597

multiple types of tagmosis and extreme modifications of the adult
body in some parasitic or sessile forms (such as barnacles or
many parasitic copepods). Traditionally, researchers focused on
either phylogenetic inquiry within ‘Crustacea’ or within Hexapoda,
until the first molecular phylogenies and mitochondrial gene rear-
rangements hinted at a paraphyletic nature of the former with
respect to the latter [78–80]. This was first taken with skepticism
but soon after, morphological evidence based largely on omma-
tidial ultrastructure, brain anatomy and patterns of neurogenesis
supported this relationship [81], and neuroanatomical support
for pancrustaceans has grown as more data have accumulated
[82]. Pancrustacea was also repeatedly recovered with strong
support using many different kinds of molecular information and
analytical approaches, and virtually all analyses using phyloge-
nomic data support its monophyly [10,11,13,45]. A few authors
continue to appeal for a clade uniting myriapods with hexapods
based on shared morphological characters [83,84], in part by di-
minishing the anatomical evidence for pancrustaceans (e.g., by
treating a set of specific, logically independent substructures of
the brain as a single vaguely defined character, ‘brain
complexity’). No molecular data of any kind have favored hexa-
pods grouping with myriapods rather than with ‘crustaceans’.
Relationships among the ‘crustacean’ lineages require further
attention but are converging towards some stable clades
(Figure 3). Of the traditionally recognized higher taxa, diverse,
morphologically varied clades such as branchiopods and mala-
costracans as well as smaller clades that had previously been
considered as relevant to crustacean origins, such as cephalocar-
ids (Figure 1J) and remipedes (Figure 1K), are each monophyletic.
On the other hand, maxillopodans, a grouping based mostly on
reduced trunk segment numbers, has been shown to be polyphy-
letic [12,33,72,85,86]. Remipedes, rather than splitting off near the
base of the pancrustacean radiation, as was suspected from their
homonomous trunk segmentation (Figure 1K), are now supported
as the sister group to hexapods [11,12,87], forming the clade
Labiocarida (named for both groups having a functional labium).
Before this relationship was detected using transcriptomes, it
was anticipated based on hemocyanin data [88]. Likewise, neuro-
anatomical data have been used to justify a clade comprising remi-
pedes, malacostracans and hexapods to the exclusion of groups
such as branchiopods and ‘‘maxillopodans’’ [89,90]. Cephalocar-
ids, branchiopods and labiocaridans together form a group named
Allotriocarida [11,12]. Although established (and repeatedly recov-
ered) with molecular data, the loss of a mandibular palp in post-
larval development provides possible morphological support for
allotriocaridans [11]. Although relationships within allotriocaridans
are sensitive to analytical methods, branchiopods are the stron-
gest candidate for sister group of Labiocarida.
Recent molecular analyses have repeatedly recovered a sister
group relationship between allotriocaridans and multicrusta-
ceans, which comprises the species-rich Malacostraca, Cope-
poda and Thecostraca [11,12,72,86]. The exact relationships of
these three taxa remain poorly understood, and morphological
synapomorphies that could be used to diagnose Multicrustacea
have not been identified. Allotriocaridans together with multi-
crustaceans constitute the clade Altocrustacea. Finally, oligos-
tracans constitute the sister group of altocrustaceans; Oligos-
traca contains several taxa once classified as maxillopodans,
such as ostracods, branchiurans (‘fish lice’), pentastomids
R598 Current Biology 29, R592–R602, June 17, 2019
Current Biology
Review
(‘‘tongue-worms’’, parasites that had also been regarded by
many as ‘protarthropods’ before sperm ultrastructure and mo-
lecular data agreed on their alliance with branchiurans), and
mystacocaridans [11,12,72,86]. The monophyly of ostracods
is, however, contradicted by some molecular datasets.
The internal relationships of branchiopods and malacostra-
cans have received recent attention using phylogenomic data
[12], but those of altocrustaceans and multicrustaceans (and
their subclades copepods and thecostracans) require detailed
attention. The phylogeny of remipedes has received consider-
able morphological and molecular attention [91,92], but phyloge-
nomic data remain scarce [11,87,93] and are restricted to two
species. Given the importance of remipedes to understand the
origins of hexapods [94], it would be important to generate better
genomic resources and for a larger number of species.
The pattern and timing of hexapod evolution have been ex-
plained with considerable confidence, especially after the use of
large numbers of genomes and transcriptomes [10]. This
approach seems to have settled old phylogenetic questions
regarding the early splits of hexapods, such as the monophyly or
paraphyly of Entognatha [95,96], Diplura [97], Zygentoma [95] or
Palaeoptera [98–100]. Phylogenomic analyses now support para-
phyly of ‘Entognatha’, hexapods with entognathous mouthparts
dividing into a clade composed of collembolans (springtails:
Figure 1L) and proturans on the one hand, but diplurans as sister
group to insects (Ectognatha) on the other. Other strong patterns
in the deep branches of the hexapod tree are monophyly of diplur-
ans, monophyly of zygentomans, and the sister group relationship
of odonates and ephemeropterans—the traditional Palaeoptera.
Likewise, within the insects, traditional clades often recovered
include Pterygota (the winged insects), Neoptera, Polyneoptera,
Condylognatha and Holometabola. Within the primitively flightless
hexapods, the recovery of the clade Ellipura (proturans and col-
lembolans) and the sister group relationship between diplurans
and insects (Cercophora) are congruent with most classical
morphological schemes, and overturn a likely spurious conflicting
result found in many early molecular phylogenies, in which protur-
ans and diplurans grouped together as Nonoculata.
A recent study, re-analyzing a published transcriptomic data
set [10] with a multispecies coalescent, recovered slightly
different relationships, notably non-monophyly of hexapods, as
remipedes appeared as the sister group of insects [101]. This
result could probably be attributed, among other things, to the
taxon sampling of non-hexapods in the original data set. Indeed,
a different analysis [11] using the same coalescent approach and
a dense sampling of crustacean lineages recovered monophyly
of hexapods for all the analyzed data matrices.
Phylogenomics has also resolved long-debated placements
within Polyneoptera, such as the position of zorapterans [102],
and within holometabolous insects, establishing that strepsipter-
ans are the closest relatives of coleopterans (beetles) [10,103],
and that hymenopterans constitute the sister group of all other
holometabolous insects [10]. Together with the large amount of
fossil information for insects [104], our current understanding
of the evolutionary chronicle of the major lineages of hexapods
in general and insects in particular is highly satisfactory.
The evolutionary success of insects is unquestionably linked
to the advantages offered by the evolution of flight [105]. The fos-
sil record of hexapods as a whole dates to the Early Devonian, in
Current Biology
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the form of crown-group collembolans. Pterygote insects are
represented by fossilized wings from the Early Carboniferous on-
wards [106]. Despite these relatively deep origins, hexapods are
rare in the fossil record between the Early Devonian and the Late
Carboniferous — this interval during which arachnids are more
commonly fossilized is called the ‘hexapod gap’ [107]. Insects
first become abundant in the Late Carboniferous, when ptery-
gotes become the dominant group.
While colonization of land and freshwater probably occurred
once in each of chelicerates and myriapods, pancrustaceans
have colonized freshwater and terrestrial environments multi-
ple times [108], in many insect lineages combining an aquatic
larval phase with an adult terrestrial phase (and many second-
ary colonizations of freshwater environments). Such an ability
to switch between such environments, which required adapta-
tion to many stresses, especially related to body support and
water loss, and perhaps only paralleled in snails and earth-
worms, may be the ultimate explanation for the large diversity
of the group (while most phylogenetic diversity in snails, clitel-
lates and pancrustaceans is marine, most species diversity is
terrestrial). Studies on arthropod terrestrialization have dis-
agreed on whether hexapods derived from a freshwater
ancestor [45], or from a marine ancestor [11]. These contrast-
ing hypotheses on the origin of hexapods have, however,
received relatively little attention to date and further study is
needed to better understand this major event in the history
of Earth’s biodiversity. Even less information is currently avail-
able about other terrestrialization events in isopods, amphi-
pods or decapod crustaceans. Studying these repeated pro-
cesses could allow us to look further into the evolutionary
pressures and opportunities for the development of additional
arthropod terrestrial faunas.
Conclusions
The use of genomics has brought considerable stability to the
arthropod phylogenetic tree, but some recalcitrant questions
remain, especially with respect to the relationships among
many arachnid orders. Others have not yet been explored in
great detail, including the interrelationships of multicrustaceans;
this involves both the identification of morphological or develop-
mental apomorphies for this grouping, as well as an open
question over how its three putative members interrelate. None-
theless, with the democratization of genome sequencing and the
development of additional bioinformatic techniques to study
genome evolution, including rare genomic events and the
repeated occurrence of whole genome duplications in chelicer-
ates [54,109] and hexapods [110], as well as with the continued
refinement of phylogenetic methods to deal with the ever-
increasing number of taxa and genes, the future of arthropod
phylogenetics looks brighter than ever. The contributions of
paleontology, morphological imaging and dating techniques,
with the recent discovery of many fossils with exceptional pres-
ervation, are likewise contributing towards piecing together an
ever more precise chronicle of arthropod evolution.
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