17 Arthropod Systematics The Comparative Study of Genomic, Anatomical, and Paleontological Information

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Ward C. Wheeler

Gonzalo Giribet

Gregory D. Edgecombe

281

Arthropods are perhaps the most diverse creatures on Earth,

with the number of known species approaching one million,

and perhaps 10 times as many left to discover. Comprised

today of Hexapoda (insects and relatives), Myriapoda (centipedes,

millipedes, and allies), Crustacea (shrimps, crabs,

lobsters, crayfish, barnacles, etc.), and Chelicerata (arachnids,

horseshoe crabs, and sea spiders), the arthropods vary over

four orders of magnitude in size (from <1 mm mites and parasitic

wasps to >4 m spider crabs), are herbivores and carnivores,

free-living and parasitic (endo and ecto), and solitary

and social, and constitute the great majority of animal biomass.

Arthropods are ubiquitous. They are found on all continents,

the deepest oceans, and highest mountains. Extinct

groups include trilobites, marrellomorphs, anomalocaridids,

and euthycarcinoids, some of which may well be equal in

taxonomic status to those we know today.

As members of the triploblastic Metazoa, arthropods are

characterized by a segmented, hardened, chitinous cuticular

exoskeleton and paired, jointed appendages. This exoskeleton

is composed of a series of dorsal, ventral, and lateral

plates that undergoes molting (ecdysis), sometimes periodically.

Primitively, arthropods share a compound eye with a

subunit structure that is unique within the animal kingdom.

The geological history of arthropods extends back over

520 million years (to the Lower Cambrian) with extinct lineages

of great diversity (e.g., trilobites). This history has

undergone several dramatic rounds of extinction and diversification,

most prominently in the Paleozoic Era near the end

of the Ordovician Period and at the Permian-Triassic boundary.

The Cambrian and Ordovician body fossil record of

arthropods is exclusively marine, but terrestrial forms (including

arachnids, millipedes, and centipedes) appear from

the Upper Silurian, more than 400 million years ago.

Relatives

The closest relatives of the arthropods are the enigmatic water

bears (Tardigrada) and velvet worms (Onychophora). All of

these animals share paired appendages and a chitinous cuticle.

There are approximately 800 species of tardigrades that

live in marine, freshwater, and terrestrial habitats. Marine

tardigrades are an important component of the meiofauna,

crawling between sand grains. Terrestrial tardigrades are

mostly found on mosses and bryophytes and may occur in

huge densities (hundreds of thousands to millions per square

meter). Tardigrades are small (between 150 and 1000 mm);

have a round mouth and four pairs of legs, the last one being

terminal; and, like arthropods and a few other phyla, grow

by molting. Terrestrial tardigrades can live in extreme environments,

surviving desiccation or freezing by entering into

cryptobiosis. The cryptobiotic stage has been recorded to last

more than 100 years, and in this stage they can be dispersed

by wind. The Onychophora are a group of exclusively terrestrial,

predatory creatures that live in humid temperate

(mostly southern hemisphere) and tropical forests of

282 The Relationships of Animals: Ecdysozoans

America, Southern Africa, Australia, and New Zealand. The

velvet worms are characterized by a soft body with pairs of

“lobopod” walking limbs, a pair of annulated antennae, jaws,

and oral (“slime”) papillae. About 150 extant species have been

named, but there were many more types including marine

“armored” or plated lobopods in the Early Paleozoic. Onychophorans

and arthropods share a dorsal heart with segmental

openings (ostia) and a unique structure of the nephridia,

the excretory organs. Lack of these organs in tardigrades may

be due to miniaturization. It is thought that Tardigrada is the

sister taxon of Arthropoda and Onychophora, the next closest

relative (Giribet et al. 1996, 2001).

It has been long thought that there was an evolutionary

progression from wormlike creatures, to lobopodous forms

like Onychophora, to modern arthropods. This was expressed

in the “Articulata” hypothesis that linked annelid

worms (polychaetes and oligochaetes, including leeches) to

Onychophora and Arthropoda. Recent work, especially from

DNA sequences, has largely replaced this view, instead allying

arthropods, tardigrades, and onychophorans with other

molting creatures such as the nematodes, kinorhynchs, and

priapulids in Ecdysozoa (after ecdysis or molting; Aguinaldo

et al. 1997, Giribet and Ribera 1998, Schmidt-Rhaesa et al.

1998), and uniting the annelids with mollusks, nemerteans,

sipunculans, and entoprocts in Trochozoa (Eernisse et al.

1992, Halanych et al. 1995, Giribet et al. 2000).

Extant Groups

The major extant arthropod groups are discussed in separate

chapters and so are only briefly discussed here.

Hexapoda

The insects are by far the most diverse known arthropod group

(but mites might come close), with hundreds of thousands of

species known to science. Hexapods are characterized by possession

of three body tagma (head, thorax, abdomen), the

second of which possesses three limb-bearing segments. Insecta

comprise most of the diversity within Hexapoda, insects

being those hexapods with an antenna developed as a

flagellum without muscles between segments. The hexapod

head (like that of crustaceans and myriapods) has a large,

generally robust mandible used for food maceration, a single

pair of sensory antennae, and both compound and simple

eyes. There are 30 commonly recognized hexapod “orders”

further organized into several higher groups: Entognatha

(those with internal mouthparts)—Protura, Diplura, and

Collembola (springtails); Archaeognatha (bristletails); Zygentoma

(silverfish); Ephemerida (mayflies), Odonata (damselflies

and dragonflies); orthopteroids—Plecoptera (stoneflies),

Embiidina (web spinners), Dermaptera (earwigs), Grylloblattaria

(ice insects), Phasmida (walking sticks), Orthoptera

(crickets, grasshoppers), Zoraptera, Isoptera (termites), Mantodea

(praying mantises), Blattaria (roaches), Mantophasmatodea;

hemipteroids—Hemiptera (true bugs and hoppers),

Thysanoptera (thrips), Psocoptera, Pthiraptera (lice); and the

Holometabola—Coleoptera (beetles), Neuroptera (lacewings,

dobsonflies, snakeflies), Hymenoptera (bees, ants, wasps),

Trichoptera, Lepidoptera (moths and butterflies), Siphonaptera

(fleas), Mecoptera (snow fleas), Strepsiptera, and

Diptera (flies). Basal hexapods (Protura, Collembola, Diplura,

Archaeognatha, and Zygentoma) are wingless, whereas the

more derived insect orders generally possess two pairs of

wings. Members of Neoptera (Pterygota—winged insects

except for the “paleopteran” ephemerids and odonates) possess

wing hinge structures that allow folding their wings back

over their abdomen. Those insects with complex development,

Holometabola, are the most diverse, with beetles leading

the way with more than 300,000 recognized species.

Insects are found over the world in terrestrial and freshwater

habitats, and many have economic importance as pests

or medical interest for causing or carrying disease. An extensive

fossil record of hexapods commences with the Devonian

collembolan Rhyniella (Whalley and Jarzembowski 1981),

through other Paleozoic and Mesozoic deposits, to the dramatic

and beautiful amber-preserved insects from Lebanon,

the Baltic, and the Dominican Republic (Carpenter 1992,

Grimaldi 2001).

Myriapoda

The centipedes, millipedes, symphylans, and pauropods are

multilegged, mostly soil-adapted creatures. Generally without

compound eyes (except for scutigeromorph centipedes)

but possessing a single pair of sensory antennae, the myriapods

are most easily recognized by their large numbers of

legs and the trunk not being differentiated into distinct tagmata.

Almost all postcephalic segments bear a single (centipedes,

pauropods, symphylans) or double (millipedes) pair

of legs, numbering into the hundreds in some taxa. These

arthropods are generally small (<5–10 cm), but there are

several dramatically larger examples (Scolopendra gigantea at

30 cm). There are four main lineages of myriapods: Diplopoda

(millipedes), Chilopoda (centipedes), Pauropoda, and

Symphyla. The basic division among myriapods lies between

Chilopoda, whose members have the genital opening at the

posterior end of the body, and the other three lineages,

grouped as Progoneata on the basis of the genital opening

being located anteriorly on the trunk, behind the second pair

of legs (Dohle 1998). The millipedes are by far the most diverse

group, with approximately 11,000 described species.

The chilopods are the other diverse group (~2,800 known

species). Pauropods and symphylans are less speciose, with

a few hundred described taxa. In general, myriapods are soil

creatures feeding on detritus, with the centipedes exclusively

predatory and possessing a modified fang and the ability to

deliver toxins to their prey. It is probable, but far from universally

agreed, that the myriapods share a single common

Arthropod Systematics 283

ancestor (Edgecombe and Giribet 2002). The movement and

connections of the head endoskeleton (the tentorium), structure

and musculature of the mandible, and most DNA sequence

evidence support the single origin of Myriapoda, but

several hypotheses place myriapod lineages with hexapods

(Kraus 1998). There are few well preserved myriapod fossils,

but the extant chilopod order Scutigeromorpha and the

diplopod group Chilognatha both have fossil representatives

from the Late Silurian (Almond 1985, Shear et al. 1998). The

extinct group Arthropleurida, thought to be members of

Diplopoda (Wilson and Shear 2000), may have reached 2 m

in length.

Crustacea

Crustaceans are perhaps the most morphologically diverse

group of arthropods (>30,000 species known), with huge

variation in numbers and morphology of appendages, body

organization (tagmosis), mode of development, and size

(<1 mm to >4 m). These creatures are generally characterized

by having two pairs of antennae (first and second), biramous

(branched) appendages, and a specialized swimming

larval stage (nauplius). They usually possess both simple

(“naupliar”) and compound eyes (the latter frequently stalked).

Like myriapods and hexapods, crustaceans possess strongly

sclerotized mandibles that are distinguished by frequently

having a segmented palp. The Crustacea are generally marine,

with several freshwater and terrestrial groups (e.g., some isopods,

the woodlice). Crustacean phylogeny is an area of active

debate with the status of some long-recognized groups

under discussion (see Schram and Koenemann, ch. 19 in this

vol.). Currently, several higher groups are recognized (Martin

and Davis 2001) with their interrelationships (and even interdigitiation)

unclear: Remipedia (12 species; Speleonectes, Lasionectes,

and three other genera), Cephalocarida (few species;

Hutchinsoniella and three other genera), Branchiopoda

(1000 species; fairy shrimp, water fleas, tadpole shrimp,

clam shrimp), Maxillopoda (10,000 species; copepods, barnacles,

ostracods, fish lice), and Malacostraca (20,000 species;

mantis shrimp, crayfish, lobsters, crabs, isopods, amphipods).

Many of the debates on crustacean relationships center on

the position of the recently discovered remipedes as either

the most basal lineage resembling, in some respects, the first

Crustacea, or a more derived position having little to do with

crustacean origins. The fossil group Phosphatocopina is probably

the earliest Crustacea or the closest relative of the extant

Crustacea (Walossek 1999), first occurring in the Lower Cambrian

in England and being known from fine preservational

quality, notably in the three-dimensional Orsten Cambrian

fauna (Mьller 1979).

Chelicerata

The sea spiders, horseshoe crabs, and arachnids are characterized

by division of body segments into two tagmata: prosoma

and opisthosoma (generally), and the first leg-bearing

head segment being modified into chelifores or chelicerae.

With the exception of horseshoe crabs (the American Limulus

and the Asian Carcinoscorpius and Tachypleus), extant chelicerates

do not possess compound eyes, and none have antennae.

Horseshoe crabs and arachnids have one pair of median

eyes, whereas sea spiders have a second pair. Of the three

main divisions of chelicerates [Pycnogonida—sea spiders

(1000 species), Xiphosura—horseshoe crabs (four species),

and Arachnida—spiders, scorpions, etc. (92,000 species)],

the sea spiders and horseshoe crabs are marine and arachnids

are terrestrial, with the exception of some groups of mites.

Many groups of Acari (mites and ticks) are parasites of plants

and animals, both vertebrates and invertebrates, and being

ecto- and endoparasitic, mostly of respiratory organs. The

arachnids are the most diverse component of the Chelicerata,

with the Acari and Araneae (spiders) constituting the vast

majority of taxa. Other arachnid groups include Opiliones

(harvestmen, daddy longlegs), Scorpiones (scorpions),

Solifugae (sun, camel, or wind spiders), Pseudoscorpiones

(“false” scorpions), Ricinulei, Palpigradi (micro-whip scorpions),

Amblypygi (tailless whip scorpions or whip spiders),

Uropygi (vinegaroons), and Schizomida. The Paleozoic eurypterids

are an aquatic (mostly brackish water) group, generally

considered to be the closest relatives of Arachnida,

although some workers consider them especially related to

scorpions (see Dunlop and Braddy 2001 for a discussion of

the evidence). The largest eurypterids are 1.8 m long, among

the largest arthropods ever. The sea spiders graze on corals,

anemones, or seaweeds and vary in size from quite small (<1

cm) to almost a meter in leg span. Horseshoe crabs and arachnids

are almost entirely predatory, with spiders the dominant

arthropod predators in many environments. Horseshoe

crabs scavenge and prey on small animals in seaweeds, and

like the Opiliones, they digest their food internally. Most

arachnids, however, digest food extraorally, ingesting their

prey in the form of digested fluids.

Fossil History and Extinct Lineages

No doubt there are more extinct lineages of arthropods than

extant. More likely than not, most will remain unknown to

science, but several major groups we do know about have a

great effect on our notions of higher level relationships among

the arthropods (living and extinct). Trilobites are among the

best-known group of extinct arthropods. First known from

the Lower Cambrian, trilobites had huge radiations in the

Paleozoic. Trilobites were an exclusively marine group

(10,000 species described) characterized by two longitudinal

furrows dividing the body into three lobes (hence the

name). The body segments are organized into three tagmata

(cephalon, thorax, pygidium). Trilobites possessed compound

eyes and a single pair of antennae and had biramous

appendages. All post-antennal appendages in trilobites are

284 The Relationships of Animals: Ecdysozoans

basically similar in structure (Whittington 1975). The imbricated

lamellar setae in the exopods suggest that trilobites

are closely related to the Chelicerata (being similar to the

book gills of Xiphosura and Eurypterida), together with

numerous other extinct lineages constituting the group

Arachnata. Anomalocaridids or Dinocarida: Radiodonta are

a group of large (up to 2 m), predatory Cambrian arthropod

relatives. With unmineralized but sclerotized cuticle, they

were known initially only by their raptorial feeding/grasping

appendages that were anterior to a circular mouth that

was surrounded by a ring of plates (Collins 1996). Their

phylogenetic affinities are uncertain, but most recent work

places them in the stem group of Arthropoda (Budd 2002),

probably more closely related to extant arthropods than are

tardigrades (Dewel et al. 1999). Marrellomorphs comprise

a clade known from the Burgess Shale (Middle Cambrian,

Canada) and Hunsrьck Slate (Lower Devonian, Germany)

that possess two pairs of antenniform limbs and two pairs

of long spines that curve back over the body. Marrella is

the most abundant arthropod in the Burgess Shale fauna

(Whittington 1971). Euthycarcinoids are an enigmatic

group that ranges from the Ordovician or Lower Silurian

to the Middle Triassic, having potential affinities with myriapods

or crustaceans (Edgecombe and Morgan 1999). They

possessed a single pair of antennae and numerous pairs of

uniramous legs. A diversity of lobopodian taxa has recently

come to light via soft-part-preserved specimens, mainly from

the Lower Cambrian of China. The marine lobopodians are

thought to be related to living terrestrial Onychophora or

Tardigrada, or some may be positioned higher on the arthropod

stem group. Several of the Cambrian lobopodians possessed

elaborate spines and armored plates (Ramskцld and

Chen 1998). The “Orsten” fauna of Sweden contains amazingly

well-preserved, three-dimensional Upper Cambrian

fossils, most importantly of basal crustacean-like taxa

(Walossek and Mьller 1998). Several of these forms (e.g.,

Martinssonia) are important to understanding the origins and

relationships of Crustacea. Among the most productive Paleozoic

fossil deposits are the Burgess Shale, Chengjiang and

Orsten (Cambrian), Rhynie Chert and Gilboa (Devonian),

and Mazon Creek (Carboniferous) deposits.

The Relationships of the Arthropod “Classes”

The question of arthropod relationships has been and is still

unsettled, despite the large effort invested by researchers.

Excellent literature sources and reviews on many issues about

arthropod relationships can be found in the recent volumes

edited by Edgecombe (1998), Fortey and Thomas (1998),

and Melic et al. (1999). These volumes complement the classical

treatises by Snodgrass (1938), Boudreaux (1979), and

Gupta (1979).

Of the living taxa (Chelicerata, Crustacea, Myriapoda,

Hexapoda), it seems clear that those groups that possess

mandibles (robust, sclerotized, chewing mouthparts), the

clade Mandibulata: Crustacea, Myriapoda, and Hexapoda,

share a unique common ancestor (fig. 17.1). The biting edge

of mandibles is formed by the same segment, the coxa, of the

same limb (third limb-bearing segment in Crustacea), with a

distinctive expression pattern of the Distal-less gene (Popadi7

et al. 1998, Scholtz et al. 1998). Within this group, things

become less clear. There are two main competing hypotheses:

Tracheata or Atelocerata (myriapods and insects) versus

Tetraconata or Pancrustacea (crustaceans and insects).

The Tracheata hypothesis is supported by some anatomical

evidence, notably the similar tentorial head endoskeleton, an

absence of limbs on the head segment (intercalary segment)

innervated by the third brain ganglia, and similar respiratory

and excretory organs (Klass and Kristensen 2001). Molecular

sequence data and an alternative set of anatomical features,

notably ommatidium structure, the optic neuropils, and neurogenesis,

support the Tetraconata hypothesis (Dohle 2001).

This is a somewhat simplistic view of arthropod relationships

that assumes that the four main classes are each

monophyletic. However, pycnogonids may challenge this

premise, and recent studies have shown them as the putative

sister group to all remaining arthropods (Zrzavэ et al.

1998, Giribet et al. 2001), in part supported by the presence

of a terminal mouth as in many other non-arthropod

ecdysozoans (Schmidt-Rhaesa et al. 1998) and absence of

arthropod-type nephridia and intersegmental tendons. Fossil

pycnogonids demonstrate their presence as far back as

the Cambrian (Waloszek and Dunlop 2002). Also, many

proponents of the Tracheata hypothesis supported myriapod

paraphyly (Snodgrass 1938, Tiegs 1947, Dohle 1965).

Paraphyly or polyphyly of crustaceans has also been proposed

(Moura and Christoffersen 1996).

Mandibulata is supported by most molecular and total

evidence analyses (Wheeler et al. 1993, Giribet and Ribera

1998, Wheeler 1998a, 1998b, Zrzavэ et al. 1998, Edgecombe

et al. 2000, Giribet et al. 2001). Alternatives to the clade

Mandibulata have also appeared based on molecular sequence

data analyses (Turbeville et al. 1991, Friedrich and

Tautz 1995, Giribet et al. 1996, Hwang et al. 2001), although

this seems to be an artifact of deficient taxonomic sampling

because most other molecular analyses support Mandibulata

(Regier and Shultz 1997, 1998). A second molecular alternative

places Chelicerata as sister to Tetraconata (Regier and

Shultz 2001, Shultz and Regier 1999), but again this result

seems to be a bias toward particular genes.

Although relationships within Mandibulata are debated,

molecular data from all sources tend to agree that crustaceans

and insects form a monophyletic group, with the exception

of some total evidence analyses (Wheeler et al. 1993, Wheeler

1998b, Edgecombe et al. 2000), but not from the most recent

one including eight genes and morphology (Giribet et al.

2001).

The addition of fossil arthropods to the phylogenetic mix

has rendered a strikingly different view from that of morArthropod

Systematics 285

phologists and molecular biologists, notably a hypothesis

uniting all arthropods with biramous appendages in a clade

named Schizoramia (Cisne 1974, Briggs et al. 1992, Budd

1996, Wills et al. 1998). Schizoramia contains the extant

crustaceans and chelicerates, as well as many extinct lineages,

including trilobites.

Monophyly versus Polyphyly

Arthropods were considered to be monophyletic since the

19th century (Siebold and Stannius 1848, Haeckel 1866) and

were treated as such by most zoologists until the mid 20th

century (Snodgrass 1938). A diphyletic current then appeared,

grouping the myriapods and hexapods together with

the velvet worms to form Uniramia, versus Trilobita, Crustacea,

and Chelicerata (Tiegs 1947, Tiegs and Manton 1958;

named TCC by Cisne 1974). The diphyletic theory relied

upon functional morphology arguments, based on the idea

that the synapomorphies defining arthropods, such as the

presence of a chitinous exoskeleton with jointed appendages

and the presence of compound eyes, were convergences due

to a similar mode of life.

The diphyletic theory further evolved into a polyphyletic

theory in which the only previous taxon to be maintained

was Uniramia. This was proposed by Manton (1964, 1973,

1977, 1979) and Anderson (1973, 1979). Manton proposed

Figure 17.1. Cladogram of

extant arthropod relationships,

after Giribet et al. (2001).

Peripatidae

Peripatopsidae

Eutardigrada

Ammotheidae

Endeis

Colossendeis

Limulus

Carcinoscorpius

Buthidae

Mygalomorphae

Mastigoproctus

Laniatores

Opilio

Nipponopsalis

Scutigeridae

Lithobius

Craterostigmus

Scolopendridae

Mecistocephalus

Chilenophilidae

Polyxenidae

Proteroiulus

Narceus

Sphaerotheriidae

Pauropodinae

Hanseniella

Scutigerella

Arthropleona

Protura

Campodeidae

Meinertellidae

Machilidae

Callibaetis

Tricholepidion

Lepismatidae

Periplaneta

Locusta

Drosophila

Japygidae

Balanidae

Hutchinsoniella

Remipedia2

Remipedia1

Remipedia3

Anostraca

Daphnia

Triops

Limnadia

Calanoida

Nebalia

Anaspides

Stomatopoda

Reptantia

Oniscidea

Pycnogonida

Chelicerata Myriapoda Tetraconata

286 The Relationships of Animals: Ecdysozoans

that the mandibles of crustaceans were not homologous to

those of insects and myriapods, although she did not indicate

an explicit relationship for the crustaceans or chelicerates.

Anderson (1979) used embryonic fate maps to suggest a close

relationship among annelids, onychophorans, and atelocerates

(insects and myriapods). Subsequently, Schram (1978) joined

the polyphyletists and used fate maps to endorse a relationship

between pycnogonids and chelicerates.

The arguments in defense of arthropod polyphyly were

not based on phylogenetic thinking or identifying alternative

sister groups to different arthropod clades and were refuted

by morphological (e.g., Weygoldt 1986, Kukalovб-Peck

1992, 1998, Shear 1992, Wдgele 1993), developmental (e.g.,

Weygoldt 1979, Panganiban et al. 1995, Popadi7 et al. 1996,

1998, Scholtz et al. 1998, Abzhanov and Kaufman 1999),

and molecular (e.g., Wheeler et al. 1993, Edgecombe et al.

2000, Giribet et al. 2001) evidence. Also recently, homeobox

genes have suggested homology between the chelicerae and

the antennae of myriapods and insects and the first antennae

of crustaceans (Damen et al. 1998, Telford and Thomas

1998, Abzhanov et al. 1999, Mittmann and Scholtz 2001).

The only recent defenses of arthropod polyphyly (Fryer 1996,

1998) have resorted to imaginary worms rather than real taxa

to force arthropod non-monophyly.

Schizoramia versus Mandibulata

With the issue of arthropod monophyly settled, arguments

about the relationships among the main arthropod lineages

grew, especially in relation to Schizoramia versus Mandibulata.

The TCC (Tiegs 1947, Cisne 1974) concept groups

extinct trilobites and allied “trilobitomorophs” with extant

chelicerates and crustaceans based on the primitive biramous

nature of their appendages (Hessler and Newman 1975, Briggs

and Fortey 1989, Bergstrцm 1992, Briggs et al. 1992, Wills

et al. 1995, 1998). This hypothesis, however, does not find

support in molecular analyses, but this is not unexpected

because TCC is based on the combinations of character states

found in the extinct fauna. The Schizoramia concept obviously

conflicts with Mandibulata (fig. 17.2), which finds

support in morphological and molecular analyses (see discussion

above).

Tracheata versus Tetraconata

Another major issue in arthropod systematics is the relative

position of the mandibulate taxa. Classically, myriapods and

insects were grouped together in Tracheata (or Atelocerata;

Snodgrass 1938, 1950, 1951, Wдgele 1993, Kraus and Kraus

1994, 1996, Kraus 1998, 2001, Wheeler 1998a, 1998b)

based on morphological evidence (see discussion above). The

addition of molecular data to study arthropod relationships,

however, suggested an alternate relationship of crustaceans

and hexapods (Boore et al. 1995, 1998, Friedrich and Tautz

1995, Giribet et al. 1996, 2001, Regier and Shultz 1997,

1998, Giribet and Ribera 1998), originally named Pancrustacea

(Zrzavэ et al. 1998) and later on formalized as Tetraconata

(Dohle 2001) in reference to the ommatidium

structure (four-part crystalline cone) shared by crustaceans

and insects.

Figure 17.2. Signal synapomorphies

for Mandibulata

(mandible, shown for the

chilopod Ethmostigmus) versus

Schizoramia (biramous

appendages, shown for the

cephalocarid Hutchinsoniella).

MANDIBULATA SCHIZORAMIA

Arthropod Systematics 287

Other aspects of heated argumentation about arthropod

evolution are the monophyly of Crustacea (see Schram and

Koenemann, ch. 19 in this vol.) and the monophyly of Myriapoda

(see Edgecombe and Giribet 2002).

Current Status and the Role of Fossils

In summary, arthropod systematists recognize the monophyly

of the group, with Euarthropoda closely related to

velvet worms (Onychophora) and water bears (Tardigrada).

The arthropods can be divided into four main lineages,

Chelicerata, Myriapoda, Crustacea, and Hexapoda, and a minor

lineage of more uncertain affinities, Pycnogonida. Agreement

about the monophyly of Mandibulata and Tetraconata

seems to emerge from combined analyses of morphology and

molecules (e.g., Giribet et al. 2001; fig. 17.1), but these groupings

are not recognized universally, especially not so when the

extinct diversity is brought into the picture. With regard to

the sea spiders, emerging evidence suggests that they could

be the sister group to the remaining arthropods, although a

relationship to chelicerates cannot be rejected.

To evaluate these and other hypotheses, we attempted

an analysis including almost 250 arthropods, living and extinct,

and other related animals, together with information

on more than 800 morphological characters and more than

2 kb (kilobases) of molecular sequence data. The aim of this

study was to bring together the vast array of information

known for extant arthropods and begin the integration of

extinct taxa.

New Analysis

Taxa

The analysis of Giribet et al. (2001) contained 54 wellsampled,

extant taxa but did not attempt any examination

of extinct lineages. Here we have enlarged the sample of living

taxa from 54 to 247, including seven Paleozoic taxa. These

extinct lineages were Trilobita, coded largely from Whittington

(1975: Olenoides); Emeraldella (from Bruton and Whittington

1983); Sidneyia (from Bruton 1981); Eurypterida, coded largely

from Selden (1981); the Devonian pycnogonid Palaeoisopus

(from Bergstrцm et al. 1980); and the putative stem group

crustacean Martinssonia (from Mьller and Walossek 1986).

Anomalocaridids are coded from Parapeytoia (Hou et al. 1995),

but the coding precedes the reinterpretation (Budd 2002) of

the grasping appendage as pre-antennal (with respect to crown

group euarthropods). These morphological data were coded

for 128 lineages, and the specific molecular taxa were treated

as exemplars, with each member of the morphologically

defined lineage (if there are several) receiving the same character

coding (see supporting materials, see Wheeler 2003).

Of the 247 total taxa, 227 were sampled for molecular data

[227 taxa for 18S ribosomal DNA (rDNA) and 135 taxa for

28S rDNA]. The remaining 20 taxa were sampled only for

morphological data, seven because they are extinct, and the

remainder due to the unavailability of sequence data.

Characters

Three sources of data were used in this study: morphological,

small subunit rDNA (18S), and large subunit (28S) rDNA. The

morphological characters include information from external

and internal anatomy, behavior, ultrastructure, gene order,

and development (see Wheeler 2003 for data). Overall, the

morphological data had 13 additive multistate and 795 nonadditive

characters. The small- and large-subunit sequence

data are the same fragments used in Giribet et al. (2001).

There were 10.7% missing and 14.5% inapplicable anatomical

cells, 8.10% missing 18S rDNA sequences, and 45.3%

missing 28S rDNA sequences (including extinct lineages).

Analysis

Morphological and molecular data were analyzed under parsimony

using the program POY (vers. 2.7; Gladstein and

Wheeler 1997–2002) on a 560 CPU PIII Linux cluster at the

American Museum of Natural History and morphological

analyses verified with NONA (vers. 2.0; Goloboff 1998).

Cladogram costs were calculated for unequal length sequences

using direct optimization (Wheeler 1996). A sensitivity

analysis (Wheeler 1995) was performed using a variety

of indel:transversion cost ratios (1:1, 2:1, 4:1, 8:1, and 16:1)

and transversion:transition costs (1:1, 2:1, 4:1, and 8:1). This

diversity of analyses was performed to assess the effects of

analytical assumptions on phylogenetic conclusions.

Results

Analysis of the living taxa data set via NONA produced 100

equally parsimonious cladograms of length 1669, consistency

index (CI) 0.60, and retention index (RI) 0.87, the strict

consensus of which is shown in figure 17.3A. The inclusion

of the seven extinct lineages resulted in 110 equally parsimonious

cladograms of length 1720 (CI, 0.58; RI, 0.87),

the strict consensus of which is shown in figure 17.3B. The

two analyses jibe nearly completely with each other except

for three areas: pycnogonids, remipedes/cephalocarids, and

tracheates.

The living-taxa-only analysis shows a rather standard

extant taxon hierarchy with the sea spiders as sister group

to a clade of Xiphosura (horseshoe crabs) + arachnids. This

is consistent with Snodgrass (1938), Wheeler et al. (1993),

and the basal placement of pycnogonids by Giribet et al.

(2001). The total taxon analysis (extinct + extant), however,

inverts this relationship, placing Pycnogonida as sister to

Figure 17.3. Phylogenetic analysis of morphological data for major groups of arthropods. (A) Extant taxa data set, and (B) extant +

extinct data sets. Cladogram realized using WINCLADA (ver. 1.0; Nixon 2002).

Lepidopleurus

Acanthochitona

Haliotis

Siphonaria

Rhabdus

Striarca

Solemya

Yoldia

Eunice

Sabella

Glycera

Chaetopterus

Lumbricus

Hirudo

Acanthobdella

Tubifex

Pycnophyes

Tubiluchus

Priapulus

LORICIFERA

Plectus

Anisakis

Brugia

Globodera

Bursaphelenchus

Desmodora

Enoplus

Mermis

Trichinella

Longidurus

Gordiusalbopunctatus

Gordiusaquaticus

Chordotes

Echiniscus

Thulinia

Hypsibius

Macrobiotus

Milnesium

Callipallene

Endeis

Achelia

Colossendeis

Limulus

Carcinoscorpius

Belisarius

Androctonus

Roncus

Americhernes

Gluvia

Eusimonia

Chanbria

Siro

Parasiro

Stylocellus

StylocellusJP

Phalangium

Ischyropsalis

Trogulus

Caddo

Zuma

Oncopus

Scotolemon

Palpigradi

Pseudocellus

Ricinoididae

Allonothrus

Acarus

Opilioacarus

Rhipicephalus

Liphistius

Aphonopelma

Nesticus

Paraphrynus

Amblypigidae

Mastigoproctus

Stenochrus

Trithyreus

Scutigera

Thereuopoda

Lithobius

Australobius

Paralamyctes

Henicops

Anopsobius

Craterostigmus

Scolopendra

Rhysida

Cryptops

Theatops

Scolopocryptops

Mecistocephalus

Pseudohimantarium

Pectiniunguis

Schendylops

Ballophilus

Ribautia

Clinopodes

Henia

Tasmanophilus

Zelanion

Aphilodon

Strigamia

Polyxenus

Pauropoda

Cylindroiulus

Proteroiulus

Thyropisthus

Spirobolus

Polydesmus

Scutigerella

Hanseniella

Acerentulus

Podura

Crossodonthina

Hypogastrura

Lepidocyrtus

Catajapyx

Metajapyx

Campodeidae

Campodea

Dilta

Petrobius

Machiloides

Allomachilis

Tricholepidion

Lepisma

Thermobius

Texoreddellia

Aeshna

Chromagrion

Libellula

Cultus

Stenonema

Mesoperlina

Megarcys

Oligotoma

Clothoda

Timema

Phyllium

Acheta

Melanoplus

Ceuthophilus

Forficula

Labidura

Grylloblatta

Mantis

Blaberus

Gromphi

BrazilTerm

Reticulotermes

Zorotypus

Cerastipsocus

Dennyus

Thysanopt

Saldula

Raphigaster

Okanagana

Spissistilus

Philaenus

Oncometopia

Sialis

Myrmeleon

Agulla

Dasymutilla

Leptothorax

Hemitaxonus

Polistes

Pfuscatus

Archaeopsylla

Ctenocephalides

Orcheopeas

Boreus

Bcoloradensi

Tipula

Drosophila

Hydropsyche

Leptocera

Papilio

Galleria

Tenebrio

Meloe

Caenocholax

Xpecki

Ephemera

Ephemerella

Speleonectes1

Speleonectes2

Speleonectes3

Hutchinsoniella

Hutchinsoniella2

Lepidurus

Branchinecta

Artemia

Limnadia

Daphnia

Euphilomedes

Rutiderma

Stenocypris

Heterocypris

Bairdia

Loxothylacus

Balanus

Lepas

Ulophysema

Berndtia

Trypetesa

Argulus

TANTULOCARIDA

Derocheilocaris

Calanus

Eucyclops

Cancrincola

Squilla

Gonodactylus

Anaspides

LOPHOGASTRIDA

MYSIDA

MICTACEA

SPELAEOGRIPHACEA

Tanaidacea

CUMACEA

Isopoda

THERMOSBAENACEA

AMPHIPODA

Stenopus

AMPHIONIDACEA

DENDROBRANCHIATA

Palaemonetes

Procaris

Nephrops

Astacus

Pugettia

Philyra

Panulirus

EUPHAUSIACEA

Nebalia

BATHYNELLACEA

Epiperipatus

Euperipatoides

Peripatopsis

INSECTS

CRUSTACEANS

MYRIAPODS

CHELICERATES

Lepidopleurus

Acanthochitona

Haliotis

Siphonaria

Rhabdus

Striarca

Solemya

Yoldia

Eunice

Sabella

Glycera

Chaetopterus

Lumbricus

Hirudo

Acanthobdella

Tubifex

Pycnophyes

Tubiluchus

Priapulus

LORICIFERA

Plectus

Anisakis

Brugia

Globodera

Bursaphelenchus

Desmodora

Enoplus

Mermis

Trichinella

Longidurus

Gordiusalbopunctatus

Gordiusaquaticus

Chordotes

Echiniscus

Thulinia

Hypsibius

Macrobiotus

Milnesium

Callipallene

Endeis

Achelia

Colossendeis

Paleoisopus

Limulus

Carcinoscorpius

Eurypterida

Belisarius

Androctonus

Roncus

Americhernes

Gluvia

Eusimonia

Chanbria

Siro

Parasiro

Stylocellus

StylocellusJP

Phalangium

Caddo

Ischyropsalis

Trogulus

Zuma

Oncopus

Scotolemon

Palpigradi

Pseudocellus

Ricinoididae

Allonothrus

Acarus

Opilioacarus

Rhipicephalus

Liphistius

Aphonopelma

Nesticus

Paraphrynus

Amblypigidae

Mastigoproctus

Stenochrus

Trithyreus

Emeraldella

Sidneyia

Scutigera

Thereuopoda

Lithobius

Australobius

Paralamyctes

Henicops

Anopsobius

Craterostigmus

Scolopendra

Rhysida

Theatops

Scolopocryptops

Cryptops

Mecistocephalus

Pseudohimantarium

Henia

Strigamia

Clinopodes

Aphilodon

Tasmanophilus

Ribautia

Zelanion

Pectiniunguis

Schendylops

Ballophilus

Polyxenus

Pauropoda

Cylindroiulus

Proteroiulus

Thyropisthus

Spirobolus

Polydesmus

Scutigerella

Hanseniella

Acerentulus

Podura

Hypogastrura

Crossodonthina

Lepidocyrtus

Catajapyx

Metajapyx

Campodeidae

Campodea

Dilta

Petrobius

Machiloides

Allomachilis

Tricholepidion

Lepisma

Thermobius

Texoreddellia

Aeshna

Chromagrion

Libellula

Ephemera

Ephemerella

Cultus

Stenonema

Mesoperlina

Megarcys

Oligotoma

Clothoda

Forficula

Labidura

Grylloblatta

Mantis

Blaberus

Gromphi

BrazilTerm

Reticulotermes

Timema

Phyllium

Acheta

Melanoplus

Ceuthophilus

Zorotypus

Cerastipsocus

Dennyus

Thysanopt

Saldula

Raphigaster

Okanagana

Spissistilus

Philaenus

Oncometopia

Sialis

Myrmeleon

Agulla

Tenebrio

Meloe

Caenocholax

Xpecki

Dasymutilla

Leptothorax

Hemitaxonus

Polistes

Pfuscatus

Archaeopsylla

Orcheopeas

Ctenocephalides

Boreus

Bcoloradensi

Tipula

Drosophila

Hydropsyche

Leptocera

Papilio

Galleria

Speleonectes1

Speleonectes2

Speleonectes3

Hutchinsoniella

Hutchinsoniella2

Squilla

Gonodactylus

Anaspides

LOPHOGASTRIDA

MYSIDA

MICTACEA

Isopoda

Tanaidacea

CUMACEA

THERMOSBAENACEA

SPELAEOGRIPHACEA

AMPHIPODA

Stenopus

EUPHAUSIACEA

AMPHIONIDACEA

DENDROBRANCHIATA

Palaemonetes

Procaris

Nephrops

Astacus

Pugettia

Philyra

Panulirus

Nebalia

BATHYNELLACEA

Lepidurus

Branchinecta

Artemia

Limnadia

Daphnia

TANTULOCARIDA

Euphilomedes

Rutiderma

Stenocypris

Heterocypris

Bairdia

Argulus

Loxothylacus

Balanus

Lepas

Ulophysema

Berndtia

Trypetesa

Derocheilocaris

Calanus

Eucyclops

Cancrincola

Martinssonia

Trilobita

Parapeytoia

Epiperipatus

Euperipatoides

Peripatopsis

INSECTS

MYRIAPODS

CRUSTACEANS

CHELICERATES

A B

288

Figure 17.4. Phylogenetic analysis of molecular data for arthropods. (A) 18S, (B) 28S, and (C) combined molecular data with indels

costing 8; transversions, 1; and transitions, 1; and morphological transformations costing 8. Cladogram realized using WINCLADA

(ver. 1.0; Nixon 2002).

Lepidopleurus

Acanthochitona

Sabella

Lumbricus

Hirudo

Acanthobdella

Tubifex

Haliotis

Siphonaria

Solemya

Eunice

Yoldia

Glycera

Striarca

Chaetopterus

Rhabdus

Pycnophyes

Gordiusalbopunctatus

Gordiusaquaticus

Chordotes

Tubiluchus

Priapulus

Euperipatoides

Epiperipatus

Plectus

Globodera

Bursaphelenchus

Anisakis

Brugia

Desmodora

Trichinella

Longidurus

Mermis

Enoplus

Podura

Hypogastrura

Crossodonthina

Lepidocyrtus

Metajapyx

Acarus

Derocheilocaris

Cerastipsocus

Dennyus

Balanus

Lepas

Loxothylacus

Pauropoda

Scutigerella

Hanseniella

Hutchinsoniella

Hutchinsoniella2

Zorotypus

Tipula

Drosophila

Acerentulus

Calanus

Cancrincola

Eucyclops

Daphnia

Branchinecta

Artemia

Lepidurus

Limnadia

Peripatopsis

Nebalia

Squilla

Gonodactylus

Isopoda

Anaspides

Palaemonetes

Procaris

Nephrops

Astacus

Panulirus

Stenopus

Pugettia

Philyra

Henicops

Catajapyx

Campodeidae

Campodea

Speleonectes1

Speleonectes2

Speleonectes3

Texoreddellia

Tanaidacea

Tricholepidion

Lepisma

Thermobius

Melanoplus

Ceuthophilus

Libellula

Aeshna

Chromagrion

Ephemera

Ephemerella

Stenonema

Xpecki

Caenocholax

Forficula

Labidura

Saldula

Raphigaster

Acheta

Phyllium

Timema

Clothoda

Oligotoma

Okanagana

Spissistilus

Philaenus

Oncometopia

Hydropsyche

Leptocera

Galleria

Papilio

Cultus

Mesoperlina

Megarcys

Meloe

Myrmeleon

Archaeopsylla

Ctenocephalides

Orcheopeas

Boreus

Bcoloradensi

Sialis

Agulla

Tenebrio

Grylloblatta

Dasymutilla

Polistes

Pfuscatus

Leptothorax

Hemitaxonus

Mantis

Blaberus

Reticulotermes

Gromphi

BrazilTerm

Argulus

Dilta

Thysanopt

Ulophysema

Berndtia

Trypetesa

Polyxenus

Euphilomedes

Rutiderma

Stenocypris

Heterocypris

Bairdia

Petrobius

Machiloides

Allomachilis

Echiniscus

Thulinia

Hypsibius

Macrobiotus

Milnesium

Allonothrus

Roncus

Americhernes

Opilioacarus

Rhipicephalus

Limulus

Carcinoscorpius

Palpigradi

Belisarius

Androctonus

Liphistius

Nesticus

Aphonopelma

Paraphrynus

Amblypigidae

Mastigoproctus

Stenochrus

Trithyreus

Ischyropsalis

Trogulus

Zuma

Oncopus

Scotolemon

Phalangium

Caddo

Siro

Parasiro

Stylocellus

StylocellusJP

Pseudocellus

Ricinoididae

Gluvia

Eusimonia

Chanbria

Callipallene

Colossendeis

Endeis

Achelia

Ribautia

Scutigera

Thereuopoda

Lithobius

Australobius

Paralamyctes

Scolopendra

Theatops

Scolopocryptops

Rhysida

Cryptops

Pectiniunguis

Schendylops

Ballophilus

Cylindroiulus

Proteroiulus

Thyropisthus

Spirobolus

Polydesmus

Mecistocephalus

Craterostigmus

Anopsobius

Pseudohimantarium

Clinopodes

Tasmanophilus

Zelanion

Aphilodon

Strigamia

Henia

Acanthochitona

Lepidopleurus

Solemya

Yoldia

Striarca

Siphonaria

Rhabdus

Tubifex

Eunice

Haliotis

Mecistocephalus

Pauropoda

Balanus

Timema

Drosophila

Tipula

Labidura

Dasymutilla

Podura

Pfuscatus

Phyllium

Hutchinsoniella2

Hemitaxonus

Dennyus

Acheta

Stenonema

Zorotypus

Petrobius

Myrmeleon

Grylloblatta

Archaeopsylla

Leptocera

Blaberus

Oligotoma

Clothoda

Agulla

Tenebrio

Artemia

Lepisma

Thermobius

Caenocholax

Xpecki

Thysanopt

Texoreddellia

Cultus

Megarcys

Oncometopia

Melanoplus

Bcoloradensi

Galleria

Papilio

Hydropsyche

Ctenocephalides

Orcheopeas

Sialis

Mantis

BrazilTerm

Tricholepidion

Dilta

Machiloides

Allomachilis

Lithobius

Australobius

Clinopodes

Strigamia

Ballophilus

Anopsobius

Peripatopsis

Speleonectes1

Speleonectes2

Speleonectes3

Achelia

Endeis

Callipallene

Colossendeis

Limulus

Carcinoscorpius

Paraphrynus

Amblypigidae

Siro

Parasiro

Ischyropsalis

Trogulus

Stylocellus

StylocellusJP

Belisarius

Androctonus

Pseudocellus

Ricinoididae

Roncus

Americhernes

Palpigradi

Phalangium

Mastigoproctus

Trithyreus

Liphistius

Nesticus

Opilioacarus

Zuma

Scotolemon

Oncopus

Caddo

Gluvia

Eusimonia

Chanbria

Scutigera

Thereuopoda

Campodeidae

Metajapyx

Polydesmus

Spirobolus

Rhipicephalus

Ribautia

Zelanion

Henicops

Cylindroiulus

Plectus

Aphonopelma

Saldula

Libellula

Acerentulus

Cryptops

Scolopocryptops

Pseudohimantarium

Schendylops

Pectiniunguis

Aphilodon

Paralamyctes

Rhysida

Craterostigmus

Theatops

Scolopendra

Tasmanophilus

Scutigerella

Hanseniella

A

B

C

Lepidopleurus

Acanthochitona

Haliotis

Eunice

Siphonaria

Rhabdus

Solemya

Glycera

Lumbricus

Hirudo

Acanthobdella

Tubifex

Yoldia

Sabella

Striarca

Chaetopterus

Pycnophyes

Gordiusalbopunctatus

Gordiusaquaticus

Chordotes

Tubiluchus

Priapulus

Echiniscus

Thulinia

Hypsibius

Macrobiotus

Milnesium

Scutigerella

Hanseniella

Hutchinsoniella

Hutchinsoniella2

Zorotypus

Thysanopt

Tipula

Drosophila

Podura

Hypogastrura

Crossodonthina

Lepidocyrtus

Plectus

Globodera

Bursaphelenchus

Anisakis

Brugia

Desmodora

Trichinella

Longidurus

Mermis

Enoplus

Allonothrus

Limulus

Carcinoscorpius

Palpigradi

Belisarius

Androctonus

Liphistius

Nesticus

Aphonopelma

Paraphrynus

Amblypigidae

Mastigoproctus

Stenochrus

Trithyreus

Ischyropsalis

Trogulus

Zuma

Oncopus

Scotolemon

Phalangium

Caddo

Siro

Parasiro

Stylocellus

StylocellusJP

Pseudocellus

Ricinoididae

Gluvia

Eusimonia

Chanbria

Roncus

Americhernes

Opilioacarus

Rhipicephalus

Callipallene

Colossendeis

Endeis

Achelia

Mecistocephalus

Euperipatoides

Spirobolus

Cylindroiulus

Proteroiulus

Thyropisthus

Polydesmus

Pectiniunguis

Schendylops

Ballophilus

Scutigera

Thereuopoda

Craterostigmus

Scolopendra

Theatops

Cryptops

Scolopocryptops

Rhysida

Lithobius

Australobius

Henicops

Anopsobius

Paralamyctes

Ribautia

Pseudohimantarium

Zelanion

Aphilodon

Clinopodes

Tasmanophilus

Strigamia

Henia

Acarus

Metajapyx

Catajapyx

Campodeidae

Campodea

Xpecki

Caenocholax

Balanus

Lepas

Loxothylacus

Speleonectes1

Speleonectes2

Speleonectes3

Daphnia

Branchinecta

Lepidurus

Limnadia

Artemia

Ulophysema

Berndtia

Trypetesa

Nebalia

Isopoda

Anaspides

Palaemonetes

Procaris

Nephrops

Astacus

Panulirus

Stenopus

Pugettia

Philyra

Squilla

Gonodactylus

Polyxenus

Pauropoda

Acerentulus

Petrobius

Stenocypris

Heterocypris

Bairdia

Euphilomedes

Rutiderma

Calanus

Cancrincola

Eucyclops

Tanaidacea

Peripatopsis

Epiperipatus

Derocheilocaris

Machiloides

Allomachilis

Argulus

Dilta

Texoreddellia

Melanoplus

Ceuthophilus

Acheta

Phyllium

Timema

BrazilTerm

Tricholepidion

Ephemera

Ephemerella

Stenonema

Okanagana

Spissistilus

Philaenus

Oncometopia

Lepisma

Thermobius

Libellula

Aeshna

Chromagrion

Clothoda

Oligotoma

Cerastipsocus

Dennyus

Forficula

Labidura

Saldula

Raphigaster

Cultus

Mesoperlina

Megarcys

Mantis

Blaberus

Gromphi

Reticulotermes

Dasymutilla

Polistes

Hemitaxonus

Pfuscatus

Leptothorax

Sialis

Tenebrio

Meloe

Agulla

Grylloblatta

Myrmeleon

Archaeopsylla

Ctenocephalides

Orcheopeas

Hydropsyche

Leptocera

Galleria

Papilio

Boreus

Bcoloradensi

289

290 The Relationships of Animals: Ecdysozoans

Figure 17.5. Sensitivity plots for (left panel) extant and (right panel) extant + extinct taxa showing the support for Tetraconata and

Tracheata over varied analytical parameter assumptions.

Arachnida, with the eurypterids, Xiphosura, trilobites, and

Emeraldella + Sidneyia as successive sister groups. The inclusion

of extinct lineages inverts the pattern based on living

taxa. This is in part because of the additional scorable states

in the pycnogonid opisthosoma due to Palaeoisopus, and the

biramous limbs of the trilobites and other basal arachnates.

A second difference comes in the basal lineages of Crustacea.

Both analyses support a major division between the

malacostracan and maxillopodan + branchiopodan lineages.

The placement of the remipedes and cephalocarids differs.

In the more restrictive analysis (extant taxa only), these two

putatively basal taxa group with Malacostraca, whereas in the

complete taxon analysis the remipedes are the sister group

to the remaining crustaceans, with Hutchinsoniella grouping

with the non-malacostracan lineages.

The highest-level disagreement between these analyses

is in the relative placement of Crustacea, Myriapoda, and

Hexapoda. The extant taxa analysis supports Crustacea +

Hexapoda (= Tetraconata), whereas the total-taxon analysis

supports Hexapoda + Myriapoda (= Tracheata). The interactions

here are complex. Certainly the role of the crustacean-

like Martinssonia as a basal mandibulate (Wдgele 1993,

Moura and Christoffersen 1996) is central. The extinct lineages

have altered the basal relationships of both the crustaceans

and the chelicerates, and therefore their basalmost

character states. Uniramy, as an example, has gone from the

primitive condition in arthropods to a derived condition

uniting tracheates on one side and arachnids + pycnogonids

on the other. This is reinforced by both Martinssonia and the

status of the anomalocarids (i.e., Parapeytoia) as sister group

to crown group Euarthropoda (Dewel et al. 1999).

Molecular analyses show a diversity of patterns depending

on the analytical parameters used to derive cladograms.

There is a general pattern, however, of linking and even intermixing

the crustacean and hexapod taxa (fig. 17.4). This

pattern has been seen in molecular analyses of arthropod data

for some time (e.g., Wheeler et al. 1993, Regier and Shultz

1997, Zrzavэ et al. 1998, Giribet et al. 2001). The four pycnogonid

representatives group together and separate from

the arachnid lineages.

Combined analyses show an interesting distinction between

extant and total-taxon analysis. As far as the relationships

among the “classes,” the extant taxa analyses are

completely robust (fig. 17.5, left panel). In each of the 20

cases examined (e.g., fig. 17.6A), the crustaceans and hexapods

form a clade. This is not terribly surprising in that both

the morphological analysis of living taxa and the molecular

data show this pattern. The Tetraconata (Dohle 2001)

[“Pancrustacea” of Zrzavэ et al. (1998) is based on crustacean

paraphyly] is ubiquitous. When the extinct taxa are included,

however, the pattern becomes less clear. At lower indel costs,

Tetraconata is favored, whereas at higher indel costs (>2:1

over base substitutions), Tracheata is most parsimonious

(figs. 17.5, right panel, and 17.6B). The “TCC” grouping was

never found. Several patterns are common to the analyses.

In both cases, the major groups (Crustacea, Chelicerata,

Myriapoda, and Hexapoda) are monophyletic. Furthermore,

the pycnogonids are brought to the base of chelicerates (sister

group to Xiphosura + Arachnida), with Emeraldella +

Sidneyia as stem-group chelicerates in the total-taxa analysis.

Both analyses also support Remipedia + Cephalocarida (found

in Giribet et al. 2001), which is not supported by either morphological

taxon set. However, this clade is sister to the remaining

crustaceans when the extinct lineages are included.

Another noteworthy difference concerns the status of the entomostracan

crustaceans, monophyletic based on the extant

taxa (see Walossek and Mьller 1998) but paraphyletic with

respect to Malacostraca when fossils are included.

Inclusion of the molecular data affects the position of some

of the extinct groups. Morphology alone resolves Trilobita

in a frequently endorsed position in an arachnate clade

(fig. 17.3B), in the chelicerate stem group (Wills et al. 1995,

1998, among many others). Analysis with the molecular data,

however, shifts the trilobites outside Arachnata (fig. 17.6B),

perhaps in part caused by character conflict when pycnogonids

are placed as sister group of euchelicerates. This latter resolution,

with trilobites as sister group to other euarthropods,

allows that the lack of differentiation of post-antennal appendages

in trilobites could be a primitive condition, rather than

the reversal forced by their deep nesting in Arachnata.

Tetraconata

(=Pancrustacea)

Tracheata

Transversion:Transition ratio

Indel cost ratio

1

2

4

8

16

1 2 4 8

Tetraconata

(=Pancrustacea)

Tracheata

Transversion:Transition ratio

Indel cost ratio

1

2

4

8

16

1 2 4 8

Arthropod Systematics 291

Figure 17.6. Combined (all data) analysis for (A) extant and (B) extant + extinct taxa with indels costing 8 transversions 1 and

transitions 1 and morphological transformations 8. Cladogram realized using WINCLADA (ver. 1.0; Nixon 2002).

Discussion

The most striking result of this analysis and summary of

current data on arthropod relationships is the importance

of extinct lineages. Although we are able to examine a great

Mollusca

Polychaeta

Clitellata

Kinorhyncha

Loricifera

Priapulida

Nematoda

Nematomorpha

Onychophora

Tardigrada

Pycnogonida

Xiphosura

Scorpiones

Palpigradi

Liphistiomorpha

Mygalomorpha

Araneomorpha

Amblypygi

Uropygi

Schizomida

Ricinulei

Parasitiformes

Opilioacarifomes

Acariformes

Sironidae

Stylocellidae

Eupnoi

Dyspnoi

Laniatores

Pseudoscorpiones

Solifugae

Collembola

Japygina

Campodeina

Protura

Archaeognatha

Tricholepidion

Zygentoma

Ephemerida

Odonata

Plecoptera

Embiidina

Grylloblattaria

Dermaptera

Mantodea

Blattaria

Isoptera

Orthoptera

Phasmida

Zoraptera

Psocodea

Phthiraptera

Thysanoptera

Hemiptera

Megaloptera

Raphidiodea

Neuroptera

Coleoptera

Strepsiptera

Hymenoptera

Siphonaptera

Mecoptera

Diptera

Trichoptera

Lepidoptera

Scutigeridae

Lithobiidae

Henicopidae

Craterostigmidae

Scolopendridae

Cryptopidae

Mecistocephalidae

Himantariidae

Dignathodontidae

Schendylidae

Ballophilidae

Geophilidae

Chilenophilidae

Aphilodontidae

Linotaeniidae

Polyxenida

Julida

Polydesmida

Spirostreptida

Spirobolida

Pauropoda

Symphyla

Nectiopoda

Stomatopoda

Anaspidacea

Bathynellacea

Lophogastrida

Mysida

Mictacea

Isopoda

Amphipoda

Cumacea

Tanaidacea

Spelaeogriphacea

Thermosbaenacea

Euphausiacea

Amphionidacea

Dendrobranchiata

Caridea

Euzygida

Reptantia

Leptostraca

Cephalocarida

Notostraca

Anostraca

Conchostraca

Cladocera

Ostracoda

Mystacocarida

Branchiura

Tantulocarida

Copepoda

Rhizocephala

Ascothoracica

Acrothoracica

Thoracica

Trilobita

Martinssonia

Paleoisopus

Eurypterida

Emeraldella

Sidneyia

Parapeytoia

Mollusca

Polychaeta

Clitellata

Kinorhyncha

Loricifera

Priapulida

Nematoda

Nematomorpha

Onychophora

Tardigrada

Pycnogonida

Xiphosura

Scorpiones

Palpigradi

Liphistiomorpha

Mygalomorpha

Araneomorpha

Amblypygi

Uropygi

Schizomida

Ricinulei

Parasitiformes

Opilioacarifomes

Acariformes

Sironidae

Stylocellidae

Eupnoi

Dyspnoi

Laniatores

Pseudoscorpiones

Solifugae

Collembola

Japygina

Campodeina

Protura

Archaeognatha

Tricholepidion

Zygentoma

Ephemerida

Odonata

Plecoptera

Embiidina

Grylloblattaria

Dermaptera

Mantodea

Blattaria

Isoptera

Orthoptera

Phasmida

Zoraptera

Psocodea

Phthiraptera

Thysanoptera

Hemiptera

Megaloptera

Raphidiodea

Neuroptera

Coleoptera

Strepsiptera

Hymenoptera

Siphonaptera

Mecoptera

Diptera

Trichoptera

Lepidoptera

Scutigeridae

Lithobiidae

Henicopidae

Craterostigmidae

Scolopendridae

Cryptopidae

Mecistocephalidae

Himantariidae

Dignathodontidae

Schendylidae

Ballophilidae

Geophilidae

Chilenophilidae

Aphilodontidae

Linotaeniidae

Polyxenida

Julida

Polydesmida

Spirostreptida

Spirobolida

Pauropoda

Symphyla

Nectiopoda

Stomatopoda

Anaspidacea

Bathynellacea

Lophogastrida

Mysida

Mictacea

Isopoda

Amphipoda

Cumacea

Tanaidacea

Spelaeogriphacea

Thermosbaenacea

Euphausiacea

Amphionidacea

Dendrobranchiata

Caridea

Euzygida

Reptantia

Leptostraca

Cephalocarida

Notostraca

Anostraca

Conchostraca

Cladocera

Ostracoda

Mystacocarida

Branchiura

Tantulocarida

Copepoda

Rhizocephala

Ascothoracica

Acrothoracica

Thoracica

INSECTS CRUSTACEANS

MYRIAPODS CHELICERATES

INSECTS MYRIAPODS CRUSTACEANS CHELICERATES

A B

deal of extant arthropod anatomy and molecular biology, the

patterns of diversification and extinction in these groups

make sampling limited to living taxa insufficient. Furthermore,

even though this initial attempt at uniting these lineages

resulted in unavoidably large levels of missing data in

292 The Relationships of Animals: Ecdysozoans

both molecular and morphological analysis, the effects of

including even a few extinct taxa were profound.

At this point, several overall patterns in arthropod relationships

can be identified as having support: monophyly of

each of the major groups, Crustacea, Myriapoda, Hexapoda,

and Chelicerata (with the possible exception of the Pycnogonida);

monophyly of Mandibulata (crustaceans, hexapods,

and myriapods); and outgroup status of Tardigrada and

Onychophora. Several other important questions remain,

including the position of the pycnogonids, the basalmost

lineages of Crustacea and the sister group to Hexapoda. As

we have shown here, these problems are sensitive to the inclusion

of extinct lineages and are unlikely to be resolved with

any great confidence until a broader sample of extinct diversity

is incorporated into this analysis. Our results changed

radically when we had 3% extinct lineages; what will happen

when we have 99%?

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