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The Palaeoscolecida and the evolution of the Ecdysozoa

Aey Yu. Zuavlev1, J Ai Gmez Viae2 a Elai Li1

1rea y Museo de Paleontologa, Departamento de Ciencias de la Tierra, Facultad de Ciencias,

Universidad de Zaragoza, C/ Pedro Cerbuna, 12, E-50009 Zaragoza, Spain2rea de Paleontologa, Departamento de Geologica, Facultad de Ciencias Biolgicas,

Univeristat de Valncia, C/ Doctor Moliner, 50, E-46100 Burjassot, SpainEmail: [email protected]

AbstrAct

Palaeoscolecidans are a key group for understanding the ear-ly evolution of the Ecdysozoa. The Palaeoscolecida possessa terminal mouth and an anus, an invertible proboscis with

pointed scalids, a thick integument of diverse plates, sensorypapillae and caudal hooks. These are features that draw asecret out of these worms, indicating palaeoscolecidan af-nities with the phylum Cephalorhyncha, which embraces

priapulids, kinorhynchs, loriciferans and nematomorphs. Atthe same time, the Palaeoscolecida share a number of char-acters with the lobopod-bearing Cambrian ecdysozoans, theXenusia. Xenusians commonly possess a terminal mouth,a proboscis (although not retractable), and a thick integu-ment of diverse plates. However, they also have telescopiclobopods similar to those of the Onychophora and the Tar-digrada. It seems likely that cephalorhynchs are descendents

of xenusians, which lost walking appendages and acquireda retractable proboscis as well as a vermifom body duringadaptation for a burrowing lifestyle. The cephalorhynchscould have evolved from limb-bearing xenusian-like ec-dysozoans via intermediate forms like the semi-burrowing

Facivermis, with lobopods surrounding a terminal mouthand a slim vermiform abdomen, and not vice versa. Tardi-grads, onychophorans and anomalocaridids may representother xenusian offsprings developed through morphologicaland behavioural evolution for interstitial, surface-dwellingand swimming lifestyles, respectively. This great variety ofCambrian transitional forms corresponds well with the Ec-dysozoa concept, whereas no such forms are found to sup-

port the Articulata hypothesis.

rsUM

Les Paloscolcides sont un groupe cl pour la comprhen-sion des dbuts de lvolution des Ecdysozoa. Les Pal-aeoscolecida possdent une bouche terminale et un anus,un proboscis inversible aux scalides pointues, un tgumentpais de plaques diverses, des papilles sensorielles et descrochets caudaux. Ceux-ci sont des traits qui tirent un secretde ces vers, ce qui indique des afnits paloscolecides avecle phylum des Cephalorhyncha qui inclut les priapulides, leskinorhynches, les loricifres et les nmatomorphes. Cepen-dant, les Palaeoscolecida ont aussi quelques-uns des mmescaractres que les Xenusia, ces cdysozaires cambriens qui

portaient des lobopodes. Les xnusiens possdent gnrale-ment une bouche terminale, un proboscis (quoique non re-tractile) et un tgument pais de plaques diverses. Cependant,ils ont aussi des lobopodes tlscopiques qui ressemblent

ceux des Onychophora et des Tardigrada. Il est trs probableque les cphalorhynches sont les descendants de xnusiensqui ont perdu des appendices locomotaires et ont acquis un

proboscis retractile de mme quun corps vermiforme pen-dant ladaptation un mode de vie fouisseur. Les cphalor-hynches auriaent pu voluer dcdysozaires xnusimorphesqui avaient des membres, via des formes intermdiairescomme Facivermis semi-fouisseur, qui a une bouche ter-minale entoure de lobopodes et un abdomen vermiformemince, et pas vice versa. Les tardigrades, les onychophoreset les anomalocaridides pourraient reprsenter dautres de-scendants xnusiens volus au moins dune volution mor-

phologique et comportementale pour la vie interstitielle, la

vie sur la surface et la vie nageante respectivement. Cettegrande varit de formes transitionnelles du Cambrien cor-respond bien lide dEcdysozoa, tandis quon na trouvaucune forme qui appuie la proposition dArticulata.

From: Johnston, P.A., and Johnston K.J. (eds.), 2011. International Conference on the Cambrian Explosion, Proceedings.Palaeontographica Canadiana No. 31: 177204. 2011 Joint Committee on Paleontological Monographs for CSPG/GAC

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PALAEONTOGRAPHICA CANADIANA, No. 31, 2011178

IntrodUctIon

For a long time, the Articulata paradigm, which assumes aunity of the Annelida and the Arthropoda, and the origin ofthe latter from annelid worms, led phylogenetic analyses(e.g., Nielsen, 1995). However, when Aguinaldo et al. (1997)assessed the phylogenetic position of nematodes using a rel-atively slowly evolving nematode complete 18S ribosomal(r) DNA gene sequencealso known as the small subunitrRNA gene, or SSU rRNAthis paradigm was questioned

because the Nematoda turned out to be closer relatives ofthe Arthropoda than were the Annelida. In this molecularresearch, the nematode Trichinella spiralis, in addition toCaenorhabdites elegans, which was common in many stud-ies, had been used to eliminate the potential analytic problemof long-branch attraction. According to comparative data on

partial gene sequences of small (18S) and large (28S) nu-clear subunits, which contain conservative areas permitting

establishment of a degree of relationships between phylo-genetically remote groups (such as classes and phyla), aswell as highly variable areas allowing clarication of afni-ties of close taxa (such as species), molluscs are united with

brachiopods, other lophophorates, nemertines, sipunculids,echiurids, pogonophorans and annelids. In turn, arthropodsare related to onychophorans, tardigrades, pentastomids, pri-apulids, kinorhynchs, nematomorphs and nematodes. Thesetwo groups represent major clades of protostomian animals:the Lophotrochozoa and the Ecdysozoa, respectively (Agui-naldo et al., 1997; Aleshin et al., 1998; Giribet, 1999; Garey,2001).

This basic subdivision of the protostomian bilaterians

has been subsequently supported by independent data sets,most notablyHox genes among which Ubx, abd-A, andAbd-B have ecdysozoan-specic peptides (de Rosa et al., 1999).Additionally, Haase et al. (2001) reported that the Ecdysozoashow common neural expression of horseradish peroxidase(HRP) immunoreactivity that is absent in other animals,and they suggested that the presence of anti-HRP-reactiveglycoprotein(s) is a synapomorphy for this clade.

Further, Anderson et al. (2004) published data from thesodium-potassium ATPase -subunit gene, which also ttedin with the Ecdysozoa hypothesis. Unfortunately, this re-search did not take annelids into consideration. Combinedmultigene studies of metazoan relationships from taxonomi-

cally well sampled molecular data sets including 18S rRNAand 28S rRNA (Mallatt and Giribet, 2006), 18S rRNA, myo-sin II, histone H3 and elongation factor 1- (Giribet, 2003),and 18S rRNA, two 28S rRNA segments, cytochrome coxidase subunit I, histone H3, and U2 small nuclear RNA(Colgan et al., 2008) also conrmed the Ecdysozoa unity.

Further support comes from investigations of complete mi-tochondrial (mt) genome sequences (Webster et al., 2006;Podsiadlowski et al., 2008); of small non-coding regulatorygenes, microRNAs, showing very low homoplasy, rare sec-ondary losses and unessential convergence (Sempere et al.,2007); and of multiple nuclear protein-encoding genes (Ba-gu et al., 2008; Bourlat et al., 2008). The data on mtDNAare especially important because this molecule is remark-ably uniform across different groups of bilaterians, whilegenes encoded in mtDNA are compactly arrayed, separatedwithoutor by only a fewnucleotides and contain neitherintrons nor regulatory sequences (Lavrov, 2007). Finally,

the Ecdysozoa were validated by expressed sequence tags(EST), which permitted a reconstruction of evolutionary re-lationships based on short fragments of hundreds of thou-sands of genes (Roeding et al., 2007; Dunn et al., 2008).These strongly expressed fragments, obtaining by sequenc-ing random clones drawn from a complementary DNA li-

brary, allow 150 genes to be identied as equivalent across asample of 71 metazoans.

However, the critics of the Ecdysozoa concept continuedto deny it as they found that the Ecdysozoa were merely amolecular clade (e.g., Wgele and Misof, 2001; Pilato et al.,2005). Also, some genome-scale analyses had claimed to

refute the Ecdysozoa hypothesis (e.g., Philip et al., 2005;Rogozin et al., 2007), but these analyses were awed ow-ing to limited taxon sampling, which included only threeor four taxa in total, and an inability to correct phylogeniesadequately for highly derived C. elegans sequences, i.e., along-branch attraction artefact (Copley et al., 2004; Philippeet al., 2005; Irimia et al., 2007).

Etymologically, the name Ecdysozoa is derived fromGreek - (which means, to take off ones cloth),hinting at a property of all members of this clade, and onlymembers of this clade to undergo a full ecdysis (to take offtheir complete cuticle), at least once during their life cycles.(Incomplete shedding, gradual shedding, or a regeneration of

tex-g. 1. Anatomy of Cambrian cephalorhynchs replaced by chlorite, Murero Lagersttte, Aragn, Spain ( A, Eupper Bilbilian Stage,Lower Cambrian. d, GCaesaraugustan Stage, Middle Cambrian) and reconstructions of developmental stages of palaeoscolecidans (b, c,F). Abody cavity in palaeoscolecidan gen., and sp. indet., MPZ 2009/1235; bMarkuelia-type embryo (based on Dong et al., 2005); cShergoldana-type larva (based on Maas et al., 2007c); d, Eimprints of intestine and retractors onto integument (arrowed) in palaescolecidanSchistoscolex sp.: dMPZ 2009/1237; EMPZ 2009/1238; Fadult palaeoscolecid (based on Mller and Hinz-Schallreuter, 1993; Han et al.,2007): 1mouth cone bearing pharyngeal sensory-masticatory teeth, 2introvert bearing sensory-locomotory scalids, 3abdomen (for thegreatest part omitted), 4plates, 5microplates, 6platelets, 7sensory papillae, 8sensory tubules, 9pore canals, 10caudal hooks; Gmid-gut diverticulae (arrowed) in cephalorhynch gen., and sp. indet., MPZ 2009/1239. Scale bar = 5 mm (A, D, E, G), 20 m (B, C), 2 mm (F).

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arthropod ground pattern and is revealed in metanaupli ofbranchiopod crustaceans, embryos of malacostracan crus-taceans, and in the development of Hexapoda and Xipho-sura (Harzsch, 2006).

The ring-type brain organization in the majority ecdyso-zoan groups is probably related to the mouth structure, which

is represented by a more or less well expressed anterior pro-boscis, commonly by a retractable one or an introvert. Theintrovert incorporates brain and inner and outer retractormuscles and is covered with numerous concentric rows ofgenerally hollow sensory-locomotory spines called scalids.The introvert, which is used for locomotion, is presentat least at a larval stagein the Priapulida, the Loricifera,the Kinorhyncha and the Nematomorpha, which Malakhov(1980; Malakhov and Adrianov, 1995) included in the phylumCephalorhyncha; Nielsen (1995) into the Introverta (includ-ing the Nematoda); and Lemburg (1999) into the Scalidopho-ra (excluding the Nematomorpha). Some nematodes possess

an introvert also (Nielsen, 1995), while pycnogonids have anon-retractile proboscis and a triradiate pharynx typical ofsome cephalorhynchs (Eriksson and Budd, 2001b; Miyazaki,2002). Tardigrades have a prominent telescoping mouth conesurrounded by a ring of plate-like peribuccal lamellae and atri-radial bucco-pharyngeal apparatus armed with teeth thatresembles a loriciferan mouth cone with its closing apparatus(collar) (Dewel and Dewel, 1997; Kristensen, 2002; Deweland Eibye-Jacobsen, 2006). If the name Proboscidea werenot afxed to a few mammalian species, it would be suitablefor the Ecdysozoanot including euarthropods.

Recent investigations on the embryogenesis of ecdysozo-

ans have revealed an absence of any traces of spiral cleavageas well as ciliated larvae and a larval apical organ, whichcharacterizes the other principal clade of protostomians, theLophotrochozoa (Nielsen, 2003; Ungerer and Scholz, 2009).The same similarities in early embryogenesis are also ob-served among the Euarthropoda, the Tardigrada, the Pycno-gonida, the Nematoda and the Priapulida. Such an early em-

bryogenesis is characterized by a holoblastic, irregular radial,equal to subequal cleavage pattern and gastrulation specied

by large, division-retarded, immigrating blastomeres fol-lowed by smaller immigrating blastomeres (Hejnol and Sch-label, 2005; Schulze and Schierenberg, 2008; Ungerer andScholz, 2009). In addition, the Ecdysozoa are direct-devel-opers, although this is not a unique feature of this clade (Slyet al., 2003).

Many more morphological features in common charac-terize stem-lineage ecdysozoans, whose fossil remains crowdCambrian strata (542490 Ma) especially in Lagerstttensuch as the Burgess Shale in Canada, Chengjiang in China,the Sirius Passet in Greenland, Sinsk in Yakutia, Russia,Murero in Spain, and some others.

the cuticle is observed in some leeches, polychaetes and gas-trotrichs [Pilato et al., 2005].) In addition to this key-feature,which is relied upon presence of certain proteins responsiblefor moulting of the cuticle, the Ecdysozoa share other com-mon morphological features that have not been treated asimportant until the present time.

These principal features common to ecdysozoan bodyanatomy and embryology include: (1) the same type ofcuticle; (2) a similar basic organisation of the nervoussystem; and (3) the same pathway of early embryogen-esis.

The ecdysozoan cuticle is differentiated into a lamel-lar epicuticle secreted by the tips of epidermal microvillifollowed by a protein-containing exocuticle and a chitin-ous (-chitin) fibrillary endocuticle. Its moulting is in-duced by ecdysone steroid hormones, as has been shown

by euarthropods, onychophorans, tardigrades, priapulids,kinorhynchs, loriciferans and nematomorphs (Robson,

1964; Crowe et al., 1970; Plotnick, 1990; Lemburg, 1995;Schmidt-Rhaesa et al., 1998; Nielsen, 2001; Schmidt-Rhaesa, 2006). Among the Nematomorpha, adults appar-ently lack cuticular chitin, but the larval cuticle is thesame as in loriciferan and priapulid larvae, and the posi-tion of chitin within the basal fibrillar cuticle layer cor-responds exactly to the location of cuticular chitin in theLoricifera and the Priapulida (Neuhaus et al., 1996). Achitinous cuticle is almost lost in the Nematoda but isstill preserved in the structure of their pharynx (Neuhauset al., 1997). By comparison, annelid cuticle is composed

principally of layers of thick oriented collagen fibers,penetrated by numerous processes from the epithelial

cells and, thus, differs radically from that of ecdysozo-ans (Robson, 1964). Chitin is apparently absent in nearlyall annelid cuticles, and it is detected in annelid chaetaein the form of -chitin only; in molluscs, bryozoans and

brachiopods, -chitin is present (Plotnick, 1990). Noneof the ecdysozoans possesses either locomotory cilia asadults or larval cilia, but this is merely a consequence ofthe presence of moulting cuticle that prevents the devel-opment of any external soft tissues or cells.

A similar basic organization of the cerebrum amongthe majority of priapulids, loriciferans, kinorhynchs,nematomorphs, nematodes, tardigrades, onychophorans

and pycnogonids is expressed in the presence of a cir-cumpharyngeal brain consisting of three successive ringsand a ventral nerve cord (Eernisse, 1997; Dewel et al.,1999; Eriksson et al., 2003; Maxmen et al., 2005; Telfordet al., 2008). Judging by this feature, the worm-like ec-dysozoans (+Gastrotricha) were even separated into the

phylum Cycloneuralia (Nielsen, 1995). Regardless of theancestral position of the mouth, an embryonic circum-oral nerve ring is thought to be most likely a part of an

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lack key synapomorphies of crown-group priapulids. For in-stance, Middle CambrianAncalagon andFieldia do not pos-sess a retractable proboscis (introvert), while all the extant

priapulids have introverts (Conway Morris, 1977; Malakhovand Adrianov, 1995). The proboscis ofAncalagon bears non-differentiated scalids that very much resemble trunk spines.

Nonetheless, the basic features of such worms as the Pal-aeoscolecida,Ancalagon andFieldia still satisfy the deni-tion of the phylum Cephalorhyncha.

Thus, the representatives of the Class PalaeoscolecidaConway Morris and Robison (1986) possess such key fea-tures of the Cephalorhyncha as an introvert bearing a termi-nal mouth as well as sensory-locomotory scalids, a straight

cAMbrIAn VErMIForMEcdYsoZoAns

cAMbrIAn cEphALorhYnchs

These are the ecdysozoan cuticles that compose a signicantpart, in terms of both biovolume and biodiversity, of Cambri-an fossils including so-called soft-bodied ones (e.g., Con-way Morris, 1986; Ivantsov et al., 2005; Dornbos and Chen,2008). Aside from arthropods, palaeoscolecidans, priapulids,other cephalorhynch worms, xenusians and anomalocari-dids represent principal groups of Cambrian ecdysozoans.It should be emphasized that many Cambrian priapulids

tex-g. 2. Muscle system of fossil and extant cephalorhynchs. Ascheme of longitudinal body section of female priapulid Tubiluchusarcticus Adrianov, Malakhov, Tchesunov and Tzetlin (modied from Malakhov and Adrianov, 1995); bpalaeoscolecidan Schistoscolex sp.,chlorite, MPZ 2006/372 (retractors of introvert are arrowed); cspiny plates from posterior end of palaeoscolecidan Wronascolex lubovae(Ivantsov and Wrona), phosphate, PIN 4349/850-1; dcircular muscle bers in abdomen of louisellian Vladipriapulus malakhovi Ivantsovand A. Zhuravlev, phosphate, PIN 4349/819-1; Etransversely arranged plates on abdomen of palaeoscolecidanPiloscolex platum Ivantsovand A. Zhuravlev, phosphate, PIN 4349/670; Fscheme of abdomen cross section of priapulidPriapulus caudatus Lamarck (modied fromMalakhov and Adrianov, 1995); Gpossible palaeoscolecidan burrow, MPZ 2009/1240. 1introvert, 2scalids, 3circumpharyngeal nervering, 4circular muscles, 5pharynx, 6retractor muscules of introvert, 7abdomen, 8longitidinal muscles, 9ventral nerve cord, 10cuticle.A, Fextant; b, GCaesaraugustan Stage, middle Cambrian, Murero Lagersttte, Aragn, Spain; cE, Botoman Stage, Lower Cambrian,Sinsk Lagersttte, Sakha-Yakutia, Russia. Scale bar = 1 cm (B, G), 500 m (A), 100 m (D, F), 10 m (C, E).

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of 20 to 50 m in size (Text-g. 2C). A primary phosphaticcomposition of palaeoscolecidan sclerites is highly probable

because even plates diagenetically altered into different clayminerals still keep traces of calcium and phosphate, whilethere is a lack of evidence for diagenetic phosphatic over-

printing (Wrona, 2004; Han et al., 2007; Gmez Vintaned

et al., 2009). In longitudinal thin sections, the cuticular platesdisplay a three-layered microstructure of an extremely thin(2 to 3 m), dense, nely laminated, outer layer characterized

by: strong birefringence of apatite crystal and C-axis orien-tation perpendicular to the surface; a somewhat thicker ho-mogenous middle layer without pronounced birefringence;and a thick basal layer penetrated by vertical canals, and withonly faint birefringence of apatite crystals indicating a weak-ly preferred orientation of C-axes parallel to the surfaces ofthe plate (Bengtson, 1977, text-g. 4; Wrona, 1982, pl. 3,gs 1a, 5.; Bendix-Almgreen and Peel, 1988, g. 7; Mrss,1988, pl. IV; Mller and Hinz, 1992, gs 14A, B, E, F; Brockand Cooper, 1993, g. 10; Text-g. 3B). The basal surface

of a plate bears a regular cross-hatching system of canals(Mller, 1973, taf. 34, g. 8a, b; Dzik, 1986, g. 7B, D; Kraftand Mergle, 1989, pl. 6, g. 4; van den Boogard, 1989, pl. 4,g. 4; Mller and Hinz, 1992, g. 14C, D).

A cuticle of similar tree-layered structure is observed ina rigid lorica of larval priapulids consisting of a thin lami-nated epicuticle, a middle homogenous layer and a thick

basal layer penetrated by vertical cuticular canals; the lat-ter is underlain by a lamina pierced by oblique longitudinalcanals housing cortical bandages consisting of collagen -

bers (Malakhov and Adrianov, 1995, g. 2.9B; Text-g. 3A).The same type of cross-hatching collagenous bers is alsoobserved in the basal layer of nematomorph cuticle (Poinar,1999, g. 4). However, the thickness of palaeoscolecid bersis two to ve times greater than that of nematomorphs (mea-sured from Mller, 1973; Dzik, 1996; Poinar, 1999, respec-tively). It should be noted that ornamentation ofHouscolexfrom the Lower Cambrian of South China (Zhang and Pratt,1996, gs 2.5, 2.6) resembles that of extant adult nemato-morphs, which is built of minute platelets or areolae (Malak-hov and Adrianov, 1995, g. 5.2A, B).

An absence of growth lines on palaeoscolecidan scleritesis indicative of animal growth by periodic moulting of thecuticle rather by an accretion of its elements. Furthermore,within a single taxon derived from the same sample unit,

there are remarkable differences in abdomen diameter, andthe smaller individuals possess the same ornamentation andarrangement of plates as the larger ones, but the interspace

between the single plates is narrower due to an incompletedevelopment of platelets. An older palaeoscolecidan cuticlewas moulted during the life of the worm and replaced bya new one formed underneath the previous cover. Exactlysuch a pattern is known in three-dimensionally preserved

palaeoscolecidans from the Middle Cambrian of Australia(Mller and Hinz-Schallreuter, 1993, text-gs 12B, 14C).

intestine, a terminal anus, caudal hooks, an abdomen withsensory spines and secretory papillae (Text-gs. 1A, DF,2B). Over the past 100 years, the Palaeoscolecida from Cam-

brian to Silurian strata were compared to the Annelida dueto a supercial resemblance of external annulation. Fromtime to time, palaeoscolecidan cuticular plates, due to their

multilayered structure, have been interpreted as scales of theoldest vertebrates (Dzik, 1996; Young et al., 1996). Since the1990s, this group is assigned either to priapulids (Dzik andKrumbiegel, 1989; Han et al., 2007) or to nematomorphs(Hou and Bergstrm, 1994; Hou et al., 2004a)despite sig-nicant differences in both of these taxaor to basal Cepha-lorhyncha/Scalidophora (Ivantsov and Zhuravlev, 2005;Maas et al., 2007a; Harvey et al., 2010).

AnAtoMY And AFFInItIEs oF thEpALAEoscoLEcIdA

Geeal Mlgy a IegumeThe long, slender vermiform transversally circular body of

palaeoscolecidans is subdivided into two principal parts:an introvert and an annulated abdomen (Text-gs. 1E, F,2B). The annulation is homonomous. The introvert differ-entiation is not well expressed. It bears a mouth cone with

papillae and a central eld with posteriorly directed senso-ry-locomotory scalids. Both these types of appendages arearranged in circles and stand alternately between adjacentrings (Han et al., 2003; Maas et al., 2007a; Conway Morrisand Peel, 2010). In papers on Cambrian palaeoscolecidans,these projections are coined variably as proboscis spinesand proboscis hooks (Han et al., 2003, text-g. 1), spines

and scalids (Maas et al., 2007a, g. 1B, C), stout spines andscalids (Conway Morris and Peel, 2010, gs. 4A, 5), re-spectively. A bursa, which is a short smooth posterior abdo-men extension, is recognizable on some palaeoscolecidansfrom the Lower Cambrian of the Sirius Passet Lagersttte(Conway Morris and Peel, 2010; g. 2C). In some pal-aeoscolecidans from the Middle Cambrian of central Aus-tralia and the Lower Cambrian of Chengjiang, the posteriorend of the abdomen is terminated with paired caudal hooks(Mller and Hinz-Schallreuter, 1993, text-g. 11B, G; Houand Bergstrm, 1994, gs 1B, 2B, 4B) as in some extant

priapulids (Malakhov and Adrianov, 1995, g. 2.3B) andlike the latero-terminal spines of kinorhynchs (Neuhausand Higgins, 2002, g. 3D; Text-g. 1F).

The cuticle is built of various tessellating sclerites in-cluding plates, microplates and platelets in descending order(Text-gs. 1F, 2B, C, E). These structures form a repeatabletransverse pattern imparting an annulated appearance to theentire abdomen. Cambrian strata beginning from the latestAtdabanian level (Cambrian Series 2, Stage 3) are abundantwith these elements known asMilaculum,Lenargyrion,Had-imopanella andKaimenella, as well as some other sclerites

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(e.g., Tubiluchus corallicola). Finally, such a combination ofthe muscle system and rigid ornamented cuticle hardly al-lowed palaeoscolecidans easy surface-dwelling excursions.

nevu syemA ventral nerve cord seems to be present in palaeoscolecidans

because their cuticles preserve a narrow longitudinal struc-ture following the entire length of the abdomen (Mller andHinz-Schallreuter, 1993, text-g. 4BD). Similarly, extant

priapulids display a distinct deviation of cuticular ornamenta-tion along the ventral nerve cord, which is usually expressed

by a paired row of scalids and other surface structures that arecrowded together (Malakhov and Adrianov, 1995, g. 2.2B).

sey oga a Gla

Sensory organs of palaeoscolecidans are represented bystructures comparable in morphology and size with oscu-lae, tubules, sensory spines and papillae of extant priapulids(Text-g. 1F). Flosculae are microscopic rounded plates witha central pore. Such microelements were gured by Mllerand Hinz (1992, g. 9C, F, I) from the Middle Cambrian ofthe Georgina Basin in Australia, although at that time, theauthors interpreted them as individual skeletal organismsand compared them to Ediacaran Dickinsonia. In fossils,sensory-glandular tubules are difcult to distinguish fromsensory spines because the former differ from the later bytheir function only. Both are elongated cones with a centralopening as in some Australian palaeoscolecidans. However,

certain smaller cones (Mller and Hinz-Schallreuter, 1993,text-g. 5E) are possible to assign to either sensory spines orto tubules, while larger annulated nipple-like structures are

probably papillae. Such structures are well known in a num-ber of phosphatized palaeoscolecidan cuticles where they aremostly restricted to the ventral side (Mller and Hinz-Schall-reuter, 1993, text-g. 13; Zhang and Pratt, 1996, gs. 2.7,2.8, 2.13). Even in non-phosphatized palaeoscolecidans,whose integuments have been replaced by clay minerals, theopenings of papillae are still recognizable on the cuticle. Be-

MuulaueThe presence of a denite introvert in palaeoscolecidansfrom Murero is indicated by traces of powerful, long, retrac-tor muscles overprinted onto the integument (Text-gs. 1E,2B). Probably, these imprints are preserved due to a thickcollagen cover of retractors like that of extant priapulids;the cover ties individual muscle bers together into thick

bunches.In palaeoscolecidans, introvert scalids are pointed back

and abdominal plates, which construct the cuticle, are or-ganized in transverse bands to resist a back movement ofthe trunk when the worm burrows through sediment (Text-gs. 2C, E). To better x the worm body, plates are arranged

by their sharp ribs normally afxed to the body axis or elsebear longer spines oriented rearward, thus, lowering the bur-

rowing load of the introvert (Mller and Hinz-Schallreuter,1993, text-g. 10H; Han et al., 2003, pl. I, g. 1ac; Ivantsovand Zhuravlev, 2005, pl. XXI). This observation is supported

by nds of palaeoscolecidans in their burrows (Zhang et al.,2006) as well as of some burrows bearing imprints of pal-aeoscolecidan cuticular bands (Text-g. 2G). Furthermore,an absence of microborings, which are common in phosphat-ic shells of coeval epibenthic animals, indicates a burrowinglifestyle for palaeoscolecidans (Zhang and Pratt, 2008).

Thus, the palaeoscolecidans must have had the same typeof hydrostatic skeleton allowing a peristaltic locomotionstyle and the same abdominal muscle system consisting oflongitudinal and circular muscles as do large extant priapu-

lids (Text-g. 2A, F). In the absence of longitudinal muscles,the worm could not burrow completely, while an absenceof circular muscles would not allow constriction of different

parts of its body to regulate the motion of liquid within thebody to create enough pressure for burrowing.

A differentiation of the abdomen ornamentation intodorsal and ventral sides (Kraft and Mergl, 1989; Han et al.,2003; Ivantsov and Zhuravlev, 2005; Conway Morris andPeel, 2010) does not contradict this lifestyle, as even in ex-tant burrowing priapulids such a differentiation is developed

tex-g. 3. Cuticle structure of extant and extinct ecdysozoans. Aextant larval priapulidHalicryptus spinulosus von Seibold (modied afterMalakhov and Adrianov, 1995), bextinct palaeoscolecidan (based on Bengtson, 1977; Dzik, 1986; Brock and Cooper, 1993); cextinctxenusian (based on Bengtson et al., 1986; Dzik, 2003). 1exocuticle, 2second layer, 3basal layer with vertical canals, 4underlying mem-

brane with horizontal canals after collagen threads. Scale bar = 20 m.

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2007a, g. 1B, C). The scalids are simple and taper to a nepoint from an expanded base (Conway Morris and Peel,2010, gs 4B, 6G).

digeive syem a by caviyIn the palaeoscolecidan digestive system, the presence of a

terminal mouth, a straight intestine and a terminal anus isestablished (Conway Morris and Robison, 1986; Barskovand Zhuravlev, 1988; Mller and Hinz-Schallreuter, 1993).The mouth leads to a retractable pharynx armed with pha-

sides, circular pores are observed in some specimens (Brockand Cooper, 1993, g. 9.14). Such pores penetrating thecuticle are known in nematodes (Wright and Hope, 1968),kinorhynchs (Malakhov and Adrianov, 1995, g. 4.3a) andtardigrades (Crowe et al., 1970).

Spine-like scalids representing sensory-locomotory ap-

pendages, papillae resembling abdominal tubules, and pha-ryngeal teeth are distinguishable in introverts of some Cam-

brian palaeoscolecidans from Chengjiang (Han et al., 2003,text-g. 1; Hou et al., 2004a, gs 11.1a, 11.5b; Maas et al.,

tex-g. 4. Cambrian xenusians. Axenusian gen., and sp. indet. showing proboscis and stubby lobopods, chlorite, MPZ 2009/1241, upper-most Bilbilian Stage, Lower Cambrian, Murero Lagersttte, Aragn, Spain; b, cxenusian gen., and sp. indet., phosphate, Botoman Stage,Lower Cambrian, Sinsk Lagersttte, Sakha-Yakutia, Russia: bannulated abdomen with lobopods, PIN 4349/820-1, ccircular muscle bersof a lobopod (a single muscle bundle is arrowed), PIN 4349/820-2. Scale bar = 1 cm (A, B), 100 m (C).

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and profusely annulated vermiform organism tightly coiledin an S-shaped or inverted S-shaped loop into a sphere, withanterior and posterior poles juxtaposed laterally. The ante-rior region exhibits a presumed terminal orice proceeded

by a smooth tapering eld, the outer rim of which is adornedwith intercalating rows of posteriorly directed conical spines,

resembling larval scalids of extant priapulids and nemato-morphs.Markuelia lauriei (Haug et al., 2009), by its minutesize (less than 320 m), is an especially plausible candidatefor a palaeoscolecidan pre-hatching larva. It possesses caudalhooks, anterior backward pointing hollow spines of a scalid-like shape, and an abdomen bearing tubules like those of lar-val priapulids. The elongated, vermiform body is folded in aglobule inside an egg-shell, which is slightly compressed. Ingeneral such an embryo resembles those of both priapulidsand nematomorphs.

If such Cambrian embryos belonged to palaeosco-lecidans, they were indeed direct developers like extantcephalorhynchs (Malakhov and Andrianov, 1995; Janssen

et al., 2009).

Afiie f palaeleia a oe Aie cea-lyThe morphological and anatomical features of the Palaeosco-lecida listed above allow us to place them within the Cepha-lorhyncha, close to the crown-group of this clade. In additionto a large number of fossils described as palaeoscolecidans,this class includes some other plate-bearing worms such asTabelliscolex, Cricocosmia, Tylotites and, possibly, Mao-tianshania from the Lower Cambrian of South China (Text-g. 5.5). The more denite position of the Palaeoscolecida

within the Cephalorhyncha is indicated by a rigid trilaminatecuticle somewhat like that of larval priapulids, by a relativelyprimitive structure of introvert, and by a number of featuresshared by palaeoscolecidans with nematomorphs (some cu-ticular structures, straight intestine, larval development), xe-nusians (cuticular microstructure and structure; see below)and even with extant onychophorans (cuticular structure andsensory papillae; e.g., V.M.St.J. Read, University Collegeof North Wales, School Animal Biology, unpublished data,1985, pls 6.23b, 6.25d), tardigrades, kinorhynchs and nema-todes (cuticular pore canals). An especially striking similar-ity is observed between palaeoscolecidan and onychophoraninteguments in both their ornamentation and size range of

cuticular elements, despite an unhardened state of the latter(e.g.,Manitouscolex in Lehnert and Kraft, 2006, g. 4.6, 4.8;andPeripatopsis in Robson, 1964, g. 2).

Such a mosaic character pattern demonstrated by pal-aeoscolecidans emphasizes their afnities with stem-lineagecephalorhynchs, abutting the crown-group, which includes

priapulids, loriciferans and nematomorphs. Hou and Berg-strm (1994) drew attention to certain similarities of pal-aeoscolecidans with adult nematomorphs, which is expressedin a slim elongated body, a rigid cuticle with cross-hatching

ryngeal, usually simple, spine-like teeth (Hou et al., 2004a,g. 11.1a; Maas et al., 2007a, g. 2B, C; Conway Morris andPeel, 2010, g. 4E).

Palaeoscolecidans from Murero demonstrate the pres-ence of a voluminous body cavity occupying the entire space

between the body wall and the intestine (Text-g. 1A). In

a single extant priapulid (Meiopriapulus), the body cavityis represented by a true coelom, while other priapulids pos-sess a haemocoel (Malakhov and Adrianov, 1995; Park et al.,2006), which is impossible to distinguish in fossil material.However, a xed axial position of the intestine in the major-ity of palaeoscolecidans (Text-g. 1D) hints at the presencein their body of supportive dorso-ventral mesenteries, whichin turn may be indicative of a coelom.

Ivantsov et al. (2005) suggested, judging by an ability ofpalaeoscolecidans to inhabit dysaerobic environments, thatthese worms relied on hemerythrin as an oxygen-transport-ing pigment similar to Recent priapulids. Without a doubt,the body cavity was lled with a liquid necessary for hydro-

static locomotion of these extinct worms.

EmygeeiA probable juvenile palaeoscolecidan, named Shergoldana,was described from the Middle Cambrian of the GeorginaBasin (Maas et al., 2007c; Text-g. 1C). By its size range,cuticular ornamentation and precise restriction to the samehorizon of the same locality where palaeoscolecidans ofthe genus Schistoscolex were discovered (Mller and Hinz-Schallreuter, 1993), it seems that Shergoldana is a juvenileform of one of them (cf. Mller and Hinz-Schallreuter, 1993,gs 10B, 11E and Maas et al., 2007c, g. 3). Shergoldana is

subdivided into a frontal region with a terminal depressionsurrounded by plicae of cuticular tissue, an annulated regioncovered with spiny plates ofSchistoscolex-type, a posteriorregion bearing structures resembling sensory papillae ofadult palaeoscolecidans, and a caudal region with a pair ofcaudal hooks. Besides, microhairs are recognisable on papil-lae, and the entire papilla is like a kinorhynch sensory spot(cf. Maas et al., 2007c, g. 4C and Malakhov and Adrianov,1995, g. 4.18). In general, this juvenile form resembles,to a certain extent, extant larval cephalorhynchs, especially

priapulids, loriciferans and nematomorphs, each of whichpossess similarly morphologically subdivided larvae. Prob-ably, Shergoldana is preserved with its introvert being fully

retracted (cf. priapulid larva in Janssen et al., 2009, g. 2F;and nematomorph larva in Malakhov and Adrianov, 1995,g. 5.12A).

Some Cambrian fossil embryos assigned to Markueliamay be related to palaeoscolecidans also (Text-g. 1B). Anumber of such embryos co-occur with palaeoscolecidansin Lower Cambrian lagersttten of the Siberian Platform(Ivantsov and Zhuravlev, 2005, pl. XIV, g. 13) and MiddleCambrian strata of the Georgina Basin (Donoghue et al.,2006; Haug et al., 2009). These are embryos of an elongate

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vanced pentaradial arrangement of the pharyngeal teeth and25-radial pattern of scalids, which is typical of many Recent

priapulids (Adrianov and Malakhov, 2001), nonetheless pos-sess rather primitive abdomens and do display a different

pattern of scalid series that occupy the anterior of the intro-vert only (Huang et al., 2004a, gs 2, 4c, d).

Larval Cambrian cephalorhynchs, having been describedrecently, are of special interest because they commonly com-

bine features of different clades. Thus, Orstenoloricus fromthe Middle Cambrian of Australia possesses an annulatedneck and an elongated sack-like abdomen formed by longi-tudinal plate-like structures and bearing several paired spine-like outgrowths (Maas et al., 2009). All these features aretypical of both priapulid and loriciferan larvae (Malakhovand Adrianov, 1995, gs. 2.38 and 3.3). However, by theirnumber, position and size, these spines are closer to larvaltubules of priapulids rather than to locomotory spines of theLoricifera. Sirilorica from the Lower Cambrian of SiriusPasset is by now the earliest representative of larval cepha-

lorhynchs (Peel, 2010). It has a lorica comparable to loricasof larval priapulids and loriciferans but 500 times longerthan that of typical loriciferans and 150 times the length of

priapulid larvae. Multicuspidate denticules preserved in acirclet just beyond the lorica can be compared in shape tothe pharyngeal teeth of larval priapulids (e.g., Malakhov andAdrianov, 1995, g. 2.37b) and to scalids in the seventh rowof loriciferan Higgins larvae (e.g., Kristensen et al., 2007,g. 5), while the sixfold symmetry of their arrangement ismore like that of the Nematomorpha.

Cambrian fossil embryos of the ecdysozoans, known asMarkuelia (Dong et al., 2005; Donoghue et al., 2006), prob-

ably belong to vermiform ecdysozoans. The oral part of em-bryos display a radial folding pattern very much resemblingthe oral cone of extant cephalorhynchs (priapulids, kino-rhynchs, loriciferans) and that of their larvae, particularlythe larvae of nematomorphs, which pass through the same

phases of embryogenesis (Malakhov and Adrianov, 1995).These embryos demonstrate a direct development, and their

post-embryonic forms, sometimes called larvae, are builtaccording to the same body plan as the adults (Donoghueet al., 2006). Also, these microfossils reveal that the mouthof the most ancient ecdysozoans developed in a terminal

position. It should be noted that even Recent crown-grouplobopodians (the Onychophora) preserve this primitive and

strikingly similar feature at early stages of their embryonicdevelopment; at later stages only, the mouth is displaced toa ventral position as in adult onychophorans and arthropods(Eriksson et al., 2003). Another interesting feature of Cam-

brian ecdysozoan embryos preserved at various successivestages (from cleavage to pre-hatching) is a central terminaldepression surrounded by a radial array of spines, which oc-curs on both ends of the embryo (Dong et al., 2005), thusdemonstrating a slight differentiation of oral and aboral endsonly. Some Cambrian adult cephalorhynchs also possess ap-

canals in the innermost layer, and caudal appendages. How-ever, adult hairworms lack any kind of pseudosegments,and their caudal hooks, which are present at the larval stageonly, are directed ventrally or posteriorly to anchor the bodyas the animal forces its way into host tissue (Poinar, 1999).On the contrary, palaeoscolecidans always bear prominent

pseudosegments, while their caudal hooks are recurved andpointed anteriorly to compensate the burrowing load of theintrovert (Text-g. 1F). Probably, the closest extant rela-tives of palaeoscolecidans are priapulids. Both classes sharea similar structure of the muscle and digestive systems, ofsensory-locomotory organs, and of glands.

Many other Cambrian cephalorhynchs, commonly treat-ed as either priapulids or nematomorphs, also lack a num-

ber of crown-group synapomorphies. The most primitiveCambrian cephalorhynchs,Ancalagon andFieldia, probablylack a retractable proboscis because they never have beenfound preserved with an inverted proboscis, and they lackimprints of retractor muscles (Conway Morris, 1977). Thus,

they should be placed at the very base of the cephalorhynchstem-lineage (Text-gs. 5.3, 5.4).

Enormous in size, Omnidens displays a mosaic set offeatures shared with larval priapulids (pharyngeal teethmorphology), as well as with kinorhynchs (placoids of theclosing apparatus of the mouth cone; cf. Malakhov andAdrianov, 1995, g. 4.5B and Hou et al., 2006, gs 4C, 6).Many other Cambrian worms possess scalids and pharyngealteeth similar to those of larval priapulids rather than to adultones (cf. Malakhov and Adrianov, 1995, g. 2.37C and Houet al., 2006, gs. 4A, 5; Maas et al., 2007a, g. 7A), andsome ancient cephalorhynchs display even more primitive

features such as a trunk covered with scalid-like spines (e.g.,Anningvermis in Huang et al., 2004b, g. 3). Besides, a num-ber of fossil cephalorhynchs (Louisella in Conway Morris,1977; Corynetis and Anningvermis in Huang et al., 2004b)

bear long spines at the anterior end that very much resembleoral stylets of the Kinorhyncha, andLouisella demonstratesa double longitudinal row of nematomorph-type natatory

bristles (Text-g. 5.6). Cambrian stem-lineage priapulids(Acosmia in Chen and Zhou, 1997; Palaeopriapulites and

Protopriapulites in Hou et al., 1999; Vladipriapulus inIvantsov and Zhuravlev, 2005), although having a true intro-vert, lack a distinct differentiation of appendages into senso-ry-locomotory scalids and sensory-masticatory teeth, while

others probably have an abdomen encased in a larval-typelorica (Palaeopriapulites,Protopriapulites) (Text-g. 2D).Finally, even cephalorhynchs approaching the priapulid

crown-group, such as Selkirkia and Ottoia (Conway Morris,1977), have pharyngeal teeth of a rather larval priapulid mor-

phology, while Ottoia,Xiaoheiqingellaand Yunnanpriapulushave a bursa at the posterior end (Conway Morris, 1977, pl.8, gs 57; caudal appendage in Huang et al., 2004a, gs 2b,4a), which is typical of larval priapulids as well. Besides,

bothXiaoheiqingella and Yunnanpriapulus, showing an ad-

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ervation and a chemical composition of fossilized midgutglands characterized by elevated calcium and phosphate insharp taphonomic contrast from immediately adjacent bodystructures (in the Murero case, clay replicas; Gmez Vin-taned et al., 2011). The preferential and rapid permineraliza-tion of these organs in phosphate is probably related to their

secretory function, to their enhanced chemical reactivity, andto an internal source of phosphate (Buttereld, 2002). Thus,contrary to Edgecombes (2009) conclusion, the presence ofmidgut glands certainly is not a derived feature of the Panar-thropoda. The latter is the clade that includes the Arthropoda,the Onychophora and the Tardigrada (Nielsen, 1995).

The trunks of the majority of xenusians are covered withthree-layered cuticular plates of absolutely similar chemicalcomposition, morphologies and microstructure, like those ofthe palaeoscolecidans (Bengtson et al., 1986, g. 3, 13; Text-g. 3C). The diversity of xenusian cuticular plates shows a

perfect parallelism with those of the palaeoscolecidans (ar-eolae in Houscolex of Zhang and Pratt, 1995, g. 2.5 andOrstenotubulus of Maas et al., 2007b, g. 4c; at knobs in

Piloscolex of Ivantsov and Zhuravlev, 2005, pl. XXI andQuadratopora of Hou and Aldridge, 2007, text-g. 5P; claw-like spines in Tylotites of Han et al., 2003, pl. I, g. 1 and

Luolishania of Ma et al., 2008, g. 4E; net-like cones in Cri-cocosmia of Han et al., 2007, g. 2 and Onychomicrodictyonof Demidenko, 2006, pl. 2; rectangular plates in Tabelliscolexof Han et al., 2007, g. 2 and Cardiodictyon of Hou et al.,2004a, g. 14.5; palaeoscolecidan genera are listed rst).

In turn, the similar cuticular structure in both groups in-dicates an alike muscular system of the body and hydrostatic

pressure-type locomotion, although with the use of walking

appendages instead of an introvert. This is not surprising,as telescopic appendages of xenusians require a hydrostaticskeleton to bear a load because the vascular system provideshydrostatic pressure, which imparts a transverse inated an-nulated appearance to the cuticle of the body and appendages(Text-g. 4B, C). A presence or, vice versa, an absence oftelescopic appendages indicates different ways of substrateoccupation rather than profound morphological differences

between xenusians and stem-group cephalorhynchs. Such in-termediate forms as Early CambrianFacivermis and Cardio-dictyon from Chengjiang and Early CambrianMureropodiafrom Murero further bridge the morphological gap betweenthese two groups (Gmez Vintaned et al., 2011).Facivermis

possesses an anterior body part bearing spiny telescopic ap-pendages like those of xenusians (e.g., Luolishania in Houet al., 2004a, g. 14.1) and a posterior part devoid of limbs

but covered with plates and hooks like those of palaeosco-lecidans; the mouth and the anus both are terminal (DelleCave and Simonetta, 1991; Zhuravlev, 1995; Liu et al., 2006;Text-g. 5.2b). Its intestine is straight, but not U-shaped as intypical sedentary animals, and with a terminal anus.

Cardiodictyon as well as many other Chinese xenusiansand Mureropodia, although bearing appendages along the

parently similar anterior and posterior ends (Huang et al.,2004a; Ivantsov and Zhuravlev, 2005). Of course, this is amorphological similarity but not a physiological one. Lateron, in the evolution of cephalorhynchs, the oral spines devel-oped into scalids and teeth of the proboscis, while those ofthe aboral end turned into caudal hooks.

The phosphatized embryos extend the fossil record of theEcdysozoa two stages down, up to the very beginning of theCambrian (ca. 15 m.y. older) and conrm the hypothesis thatthe latest common ancestor of the crown-group ecdysozoanswas a direct developer.

othEr cAMbrIAn VErMIForM EcdYsoZoAnsAnd thEIr rELAtIonshIps

None of the extant cephalorhynchs lacks an introvert, atleast at a larval stage. Only some their Cambrian relatives,namelyAncalagon andFieldia, have a non-retractable pro-

boscis among vermiform fossils. However, Cambrian strataare relatively rich in ecdysozoan fossils possessing a non-re-tractable proboscis and legs (Text-g. 5.2a). The later groupof extinct ecdysozoans is coined either the class Xenusia(Dzik and Krumbiegel, 1989) or the phylum Tardypolypoda(Chen and Zhou, 1997) and is usually shoehorned into theOnychophora and even into the Panarthropoda, despite anabsence of key panarthropod features such as a ventrallylocated mouth and pre-oral appendages including antennae(Zhuravlev, 2005). Only Luolishania (=Miraluolishania)

possesses a head with putative antenniform limbs and eyes,but it still has a terminal rather than an antero-ventral mouthand a proboscis-like extension of the gut (Liu et al., 2004; Ma

et al., 2009). Interestingly, antenniform limbs are expressedas a highly mutable feature of xenusians, being present inOnychodictyon ferox but absent in closely related O. gracilis(Liu et al., 2008). All other xenusians, which are preservedas complete body fossils, except forMegadictyon, posses aterminal mouth located on a proboscis-like extension (Whit-tington, 1978; Ma et al., 2009). In some of them, the pro-

boscis is as prominent as in Cambrian cephalorhynchs (e.g.,Xenusion in Dzik and Krumbiegel, 1989).

Both palaeoscolecidans and xenusians usually share astraight gut, a terminal anus and a spacious body cavity (Houet al., 2004b; Ma et al., 2009). Additionally, three-dimension-ally preserved, serially repeated, paired, axial structures are

observed in a Middle Cambrian cephalorhynch worm fromMurero (Text-g. 1G). These structures very much resemblemidgut glands of some Cambrian stem-lineage euarthro-

pods and anomalocaridids (e.g.,Leanchoilia,Laggania andOpabinia from the Burgess Shale; Buttereld, 2002, g. 4;Zhang and Briggs, 2007, g. 1), as well as diverticulae ofxenusians (Kerygmachela andPambdelurion in Budd, 1997,g. 11.9;Jianshanopodia in Liu et al., 2006b, g. 3B2, C1;

Magadictyon [sic] in Liu et al., 2007, Text-g. 2L, M). Also,all of these fossils are characterized by similar relief pres-

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related to a transition from a life in an open space to cryp-tic fossorial habitats, such as burrows and organic litter, andusually was accompanied by axial elongation of the trunkand polymerization of body segments. These are not occa-sional coincidences as an anterior expansion of domains ofexpression of midbody Hox genes may simultaneously ac-

count for all three morphogenic processes, namely limb loss,trunk elongation and polymerization of segments (Cohn andTickle, 1999; Greene and Cundall, 2000). It is noteworthy,that fossorial amphisbaenians or worm lizards even obtainedan integument ornamentation supercially resembling thatof palaeoscolecidans, including transverse annuli and an in-ner brous layer, probably due to a similar type of burrowing

by rapid movement of shorting and widening of transverseannuli (Lee, 2000). (An incomplete helminthization, withouta loss of appendages, is observed among myriapods; Shcher-

bakov, 1999.)However, what is in common between the Vertebrata and

the Ecdysozoa? Of course, the same groups of homeobox

regulatory genes, which are responsible for the developmentof appendages in such now remote clades as deuterostomesand protostomes (the same genes are expressed in the devel-opment of ampullae in tunicates, of tube feet in echinodermsand of parapodia in annelids). In all the bilaterians, the de-velopment of limbs is a result of the expression within thesame orthogonal axis of an integrated three dimensional pat-terning system of homologous Hox genes (Distal-less/Dlx,hedgehog/Sonic hedgehog, decapentaplegic/bone morpho-

genetic proteins, andfringe/Radical fringe in euarthropods/vertebrates, respectively) (Tabin et al., 1999). Among primi-tive chordates, the same family of the Hox genes controlsthe development of branchial arches. Thus, it is not surpris-ing that branchial arches are discovered in the earliest stem-lineage chordates from the Lower Cambrian of Chengjiang(Hou et al., 2002; Shu et al., 2003).

As a result, the cephalorhynchs were the ones that origi-nated from the xenusians via such intermediate forms as

Facivermis, and not vice versa. This morphologic and ge-netic observations are supported by the palaeoichnologicalrecord, in which the rst arthropod-type trace fossils (Mono-morphichnus lineatus) are recorded in lowermost Cambrianstrata together with Phycodes pedum and apparently pre-date the increase in tiering complexity and burrowing depthof infaunal communities, in which burrowing vermiform

animals played a main role (Droser and Li, 2001; Jensen,2003; Gmez Vintaned and Lin, 2007). Ediacaran and pre-Ediacaran trace fossils were hardly made by any group ofPhanerozoic-type multicellular animals but rather by diverseunicellular and non-Metazoan multicellular organisms (Matzet al., 2008; Zhuravlev et al., 2009). An exploitation of bur-rowing, which is certainly not a primitive lifestyle, caused adevelopment of such a complicated organ as the introvert andcontemporary loss of appendages, some of which turned intosensory papillae. Sensory papillae on the palaeoscolecidan

entire trunk, were hardly able to use them for locomotionon the sediment surface, as the appendages of the rst ofthem were disproportionately long and thin (Hou et al.,1991, 1999), while those of the latter were too short (Text-g. 4A). It should be noted that no fossil xenusians werefound with retracted lobopods, while in extant velvet worms

compressed and attened in taphonomic experiments, lobo-pods always preserve a stubby shape (Monge-Njera andHou, 2002). Worm-like crawling rather than walking would

be more suitable for animals possessing such a ratio of bodywidth to appendage length. This suggestion is conrmed bya restudy of Chinese Lower Cambrian Luolishania, which

possessed slim appendages spread horizontally (Ma et al.,2009), and by the discovery of the three-dimensionally pre-served, Orsten-type, phosphatized xenusian Orstenotubulusfrom the Middle Cambrian of Sweden, whose lobopods were

pointed laterally (Maas et al., 2007b). Besides, the latter dis-plays a striking mosaic character pattern shared with fossilpalaeoscolecidans (areolae and sensory papillae), as well

as with extant priapulids (sensory papillae), nematomorphs(areolae and single gonopore), onychophorans (areolae andsensory papillae) and tardigrades (single gonopore). Well de-veloped peripheral circular and longitudinal trunk muscula-ture in some xenusians may indicate a preference for using asinuous vermiform-type movement by these animals (Budd,1998; Zhuravlev, 2005). Judging by the trace fossil record,

possible walking lobopod-bearing animals appeared only inthe Middle Cambrian (Lane et al., 2003).

In phylogenetic reconstructions, Cambrian cephalor-hynchs are placed unanimously at the base of a phylogenetictree leading independently to arthropods via xenusians, ony-

chophorans and anomalocaridids, depending on a taxonomictreatment of these worms as either annelids or as priapulids,and on the evolution of tubules into walking lobopods onthe ventral side and into defensive spines on the dorsal side(e.g., Dzik and Krumbiegel, 1989; Conway Morris, 2000;Budd, 2001b, 2008; Zhang and Briggs, 2007). Such a unityof views clearly reects an ignorance of proper features ofthese fossils rather than good agreement of different scientif-ic approaches. Is it really possible to breed an arthropod-likecreature moving on a substrate with the help of its pivot-jointappendages (even an onychophoran-like one with lobopods)from a worm moving through the substrate by the hydro-static action of its introvert, which, due to its musculature

arrangement and rigid cuticular armour, would be absolutelyhelpless on the sediment surface?On the contrary, during the evolution of life, animals lost

their appendages many times. For instance, among variousfamilies of extant squamates (lizards and snakes), limb re-duction and limb loss are observed at least 62 times in 53different lineages, while in all the vertebrates being taken to-getherfrom ancient amphibians to cetaceansthe append-ages were lost more than 100 times (Greer, 1991; Caldwell,2003). Generally, the phenomenon of helminthization was

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blastopore (Malakhov, 2004). This hypothesis is consistentwith the analysis of transcription factors in larval develop-ment, which also indicates that primitive bilaterians wereholobenthic animals, while complex life cycles including a

planktotrophic larva evolved independently multiple times(Dunn et al., 2007; Raff, 2008). Combined sources of avail-

able information from classical morphology, developmen-tal biology, various molecular phylogenetic analyses, andwhole genomic organization make it possible to hypothesizethat ancestors of the Bilateria were bilaterally symmetrical(this is clear enough), triploblastic, probably serially iter-ated animals, with both anterior/posterior and dorsal/ventral

polarities, and possessing anterior nerve cell concentrationsand muscle cells of mesodermal afnities (Balavoine andAdoutte, 2003; Budd and Jensen, 2004; Malakhov, 2004;Finnerty et al., 2004; Boero et al., 2007; Gabriel and Gold-stein, 2007). Furthermore, it is suggested that this Urbilat-erian ancestor may have even borne appendages (Panganibanet al., 1997; Shubin et al., 1997; Balavoine and Adoutte,2003; Jacobs et al., 2007; Prpic, 2008). These may be thetype of appendages resembling, to a certain extent, cnidariantentacles that are observed in some xenusians.

As already emphasized above, data from developmentalgenetics hint at the presence of appendages in a common an-cestor of all the bilaterians (Panganiban et al., 1997; Tabinet al., 1999; Prpic, 2008). At rst glance, these data contra-dict widespread hypotheses that root the bilaterian phyloge-netic tree at microscopic multicellular precursors of the sizeof planktic or meiobenthic animals. However, principal bodysystems of bilaterians, such as musculature, a blood vascularsystem, excretory nephridia and a coelom could hardly have

evolved in microscopic metazoans (Budd and Jensen, 2004).Indeed, evidence from molecular biology, comparative anat-omy and embryology indicates that interstitial animals suchas tardigrades, kinorhynchs, loriciferans and others acquiredtheir primitive characters as a result of secondary reductionand loss of a number of features during adaptations for life inmicrospace (Lorenzen, 1985; Westheide, 1987; Higgins andThiel, 1988; Dewel and Dewel, 1997; Valentine et al., 1999;Aleshin and Petrov, 2002) and a pseudocoelomate appear-ance could be the result of coelom reduction (Rieger et al.,1991).

Also, developmental genetics data clarify that larval de-velopment in distant clades such as molluscs and echino-

derms is not expressed byHox orthologs (Dunn et al., 2007).These larvae, despite a certain morphological resemblance(topologically similar apical turf and ciliated band), were lateconvergent innovations intercalated multiple times indepen-dently into already existing direct-developing strategies evenwithin phylogenetically remote lineages (Sly et al., 2003;Dunn et al., 2007). Thus, the common Urbilaterian ancestorhardly was a microscopic planktic animal.

In turn, it is difcult to exclude that the rst cnidarianscould be descendents of the bilaterians, which were adapted

ventral side differ from lobopods by a smaller size only.Even in Recent priapulids, papillae still preserve the mor-

phology of lobopods (e.g., Malakhov and Adrianov, 1995,g. 2.17A). It is not surprisipaung that both these organs areexpressed by the same set of regulatory genes (Jacobs et al.,2007). In turn, the cephalorhynch scalids can be derivates of

xenusian lobopod claws with which they are morphological-ly and, probably, structurally similar (e.g., Lemburg, 1995,g. 3C). In many xenusians, such claws were used for an-choring either to substrate or to a host animal (Whittington,1978; Chen and Zhou, 1997).

The data on the stratigraphic distribution of vermiformecdysozoans do not contradict the idea of their origin fromxenusians. The rst denite xenusian plates (Quadrato-

pora; Microdictyon tenuiporatum in Bengtson et al., 1986)appeared in the fossil record by the end of the TommotianStage (Cambrian Series 1, Stage 2), one stage earlier thanthe rst palaeoscolecidan plates and body fossils. More-over, phosphatized xenusian claws are well known under the

names Mongolodus and Maldeotaia from the very base ofthe Cambrian Stage 1 (the Nemakit-Daldynian Stage; Roza-nov and Zhuravlev, 1992, g. 11). Also, these microfossils,although compared to chaetognathan grasping spines (Van-nier et al., 2007), very much resemble in size and morphol-ogy the claws and jaws of extant onychophorans (Robson,1964, g. 3E, F).

phYLoGEnEtIc rELAtIonshIpsAMonG thE EcdYsoZoA

Text-gure 5 summarizes morphological, anatomical, em-

bryological and molecular data on ecdysozoans discussed inthis paper with some backward extrapolations. This is not astrict, formal cladistic assessment because broad evolution-ary innovations hardly develop in accordance with cladisticrules.

Node (0) further extrapolates the idea on the origin ofthe Bilateria from a bilateral holobenthic ancestor and placesthis clade within the Eumycetozoasocial amoebas thatalready obtained regulatory homeobox genes for anterior-

posterior partitioning (Han and Firtel, 1998). Such commonepibenthic mobile antecedents probably made some tracesin sediments of ca. 1,700 Ma (Bengtson et al., 2007). Actu-ally, the origin of the appendages is merely explicated by a

duplicate expression of the family of regulatory homeoboxgenes already involved in growth and in anterior-posterior

patterning, when these genes are expressed along multipleaxes divergent from the main body axis (Minelli, 2003).

Node (1) shows the position of the Urbilaterian ancestor.Classical comparative anatomy and embryology criteria in-dicate that the ventral side of all the adult bilaterians, exclud-ing the chordates, originated from the blastoporal surface oftheir predecessors, while the mouth and the anus developedfrom the anterior and posterior extremities of an elongated

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Node (4), the Ancalagonia clade, shows further develop-ment of the cephalorhynch Bauplan as indicated by differ-entiation of sensory-locomotory papillae into anterior andabdominal areas.

Node (5) xes the Palaeoscolecida clade, which displaysthe entire set of basic cephalorhynch characters, including a

retractable proboscis (introvert) with scalids, retractor andprotractor(?) muscles, caudal hooks/bursa, and probably aseptum separating the introvert and the abdomen; sensory-locomotory structures are represented by scalids, papillae,spines, tubules and osculae; larvae possessed placoids onthe closing apparatus of the mouth cone.

Node (6), represented by the Louselliai clade, indicatessome simplication of the cuticle, although palaeoscolecid-type plates cover the abdomen of these worms, and a regular

pattern of introvert sensory-locomotory structures (scalids,etc.) is expressed.

Node (7) exposes the rst cephalorhynch crown-group,the Priapulida, the majority of which have lost the coelom

and preserve a rigid, but not biomineralized, cuticle (lorica)at the larval stage only; the body acquired a distinct sub-division into an introvert, a neck and an abdomen (includ-ing larva; Janssen et al., 2009); the pentaradially arranged

pharyngeal teeth are highly differentiated; the primary (an-teriormost) scalids, innervated directly from the circumpha-ryngeal brain, display an octaradial symmetry; and scalidsare organized into a complicated 25-radial pattern along the

body axis, which actually is a combination of nana-, octa-,and octaradial (9+8+8) symmetries (Adrianov and Malak-hov, 2001). The cephalic nervous system of priapulids isinterpreted by Eriksson and Budd (2001) as derived from

the circumpharyngeal ring that characterizes the ecdysozoanclade. Molecular studies have shown that priapulids are basalwithin the crown-group cephalorhynchs but at the same timecan be polyphyletic with coelomate (Meiopriapulus) and

pseudocoelomate clades (Garey, 2001; Webster et al., 2006).Judging by molecular analysis,Meiopriapulus always formsa clade with the Onychophora (Park et al., 2006), and it isdifcult to exclude the coelom as a symplesiomorphic char-acter of this priapulid, inherited from xenusian ancestors.

Node (8) denotes the Loricifera, whose morphology andanatomy, including the presence of a lorica, very much re-semble those of larvae of a dwarfed priapulid (Tubiluchus),thus indicating a possibility of a neotenic origin of loricifer-

ans from priapulids (Malakhov and Adrianov, 1995). Findsof Cambrian larval cephalorhynchs such as Orstenoloricusand Sirilorica, which possess features of both priapulidsand loriciferans, further support this suggestion (Maas et al.,2009; Peel, 2010). Loriciferans being interstitial predatorsobtained a buccal canal armed with oral stylets supported bymuscles, a hexaradial suctorial pharynx and a further differ-entiated system of retractor muscles, while circular-longitu-dinal peripheral musculature is reduced and protonephridiamoved inside the gonads (Kristensen, 2002).

to a passive sedentary lifestyle that turned their ventral sideup (Jgersten, 1955, 1959). The presently available data onthe cnidarian Hox gene expression pattern, although beingequivocal, do not contradict at least such a possibility (Ballet al., 2007). Fossil ecdysozoans allow a further reconstruc-tion of some deep basic features of the Bilateria, including

serially repeated (but not necessarily metameric) body unitswith blocks of circular muscles, a body cavity (possibly acoelom, relics of which are preserved in such remote cladesas some priapulids and euarthropods; Strch et al., 1989)with an open circulatory system, a nervous system that con-sisted of a pre-esophageal structure and a ventral cord, anda tubular intestine with a terminal mouth and an anus. Ex-tant onychophorans and tardigrades still keep many of these

primitive (=symplesiomorphic) features.Node (2) is the Ur-Ecdysozoa, which are represented in

the fossil record by the Early to Middle Cambrian Xenusia(as cuticular derivates from the very base of the Cambrianand as body fossils from the late Atdabanian Stage/Cambrian

Series 2, Stage 3). The xenusian ground plan includes: a seg-mented vermiform body lacking tagmosis; a non-retractable

proboscis; paired lobopod appendages pointed laterally andequipped with terminal claws; a three-laminated chitinous-

phosphate cuticle displaying a repeated anatomical pattern-ing; a straight digestive tract with both a terminal mouth andan anus and axial paired midgut diverticulae; a nervous sys-tem, probably consisting of a circumpharyngeal brain ringand a ventral cord with paired ganglia (the latter, possibly,has been documented in Paucipodia; Hou et al., 2004b), avoluminous body cavity of a probably coelomic type sur-rounded by peripheral circular and longitudinal cross-stri-

ated musculature in addition to which diagonally orientedbers might be developed (evident inPambdelurion; Budd,1998 and inPaucipodia; Hou et al., 2004b); and a direct em-

bryonic development. It is highly probable that a coelom isa plesiomorphic state of xenusians because it is preservedin onychophorans and euarthropods (during embryogenesisand as sacculi in adults) and in the priapulid Meiopriapu-lis (around the foregut) (Strch et al., 1989; Eriksson et al.,2003; Schmidt-Rhaesa, 2006). Extant lobopodian and vermi-form ecdysozoans still share a number of ne details in bothfunctional and morphological appearances, such as sensory

papillae (Robson, 1964, gs 3D, 4D; Malakhov and Adri-anov, 1995, gs 2.15E, 2.17), which very likely are derivates

of similar structures in their common ancestors, the xenu-sians.Node (3) points to the most primitive cephalorhynchs of

the Fieldiai clade typied by a loss of lobopod appendages,some of which are preserved as sensory-locomotory papil-lae, along with lobopod claws, possibly preserved as teeth, aloss of the circulatory system and appearance of the retract-able mouth cone. (The Fieldiai class as well as the Ancala-gonia and the Louselliai were established by Malakhov andAdrianov, 1995.)

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vergently as a consequence of sclerotization and miniaturiza-tion. Besides, embryologic studies have revealed neither aeuarthropod-type sequential development of trunk segmentsincluding the somites and limb buds nor the presence of agrowth zone (Hejnol and Schnabel, 2005). Tardigrades sharea number of symplesiomorphic characters, including the

ventral nerve cord of paired ganglia, the circumpharyngealbrain, and sensory papillae with kinorhynchs; and the cu-ticular columns with nematomorphs and nematodes (Croweet al., 1970; Dewel and Dewel, 1997); their spermatozoado possess some similarity in ultrastructure to those of theKinorhyncha, the Priapulida and the Loricifera (Heiner et al.,2009). Besides, tardigrades have a prominent telescopingmouth cone surrounded by a ring of plate-like peribuccallamellae and a tri-radial bucco-pharyngeal apparatus armedwith teeth (Dewel and Eibye-Jacobsen, 2006). This structurewas compared to the mouth cone and the closing apparatusof loriciferans (Kristensen, 2002) and considered to be ho-mologous to the circumoral ring of onychophorans and to

the ring of radiating plates of anomalocaridids (Dewel andEibye-Jacobsen, 2006). Although the later authors suggestedthat this is a synapomorphic feature of the Panarthropoda, the

possible presence of a similar bucco-pharyngeal apparatus inthe xenusian Kerygmachela and in the stem-lineage cepha-lorhynch Omnidens (Budd, 2001b, g. 7; Hou et al., 2006,gs. 4C, 6) may be indicative of its symplesiomorphic ratherthan synapomorphic character. It is interesting to note that inadvanced herbivorous tardigrades, only the mouth occupiesan antero-ventral position, but not as extremely so as in adultonychophorans, while carnivorous and omnivorous tardi-grades possess a terminal mouth opening (Morgan, 1982). A

presumed internalization of the formers anterior limbs intoa buccal cavity to form a stylet apparatus (Dewel and Eib-ye-Jacobsen, 2006) overprinted bilateral symmetry onto the

probably primary tri-radial symmetry of the mouth apparatusin the early evolution of the Tardigrada. As a result, a pair ofunique mouth stylets appeared during internalization of anappendage-bearing segment into a buccal cavity, like those ofthe Onychophora (Mayer and Koch, 2005; Dewel and Eibye-Jacobsen, 2006), and is probably homologous with lobopodterminal claws.

There is no evidence for a tripartite/three-segmentedbrain organization among the Tardigrada, which commonlyis cited as a principal euarthropod/tardigrade synapomorphy;

on the contrary, their brain anatomy data indicate a compact,complete, unsegmented, circumpharyngeal ring composedof bers and nerve cell perikaria resembling the conditionsin cephalorhynchs and nematodes (Zantke et al., 2008). Themedian part of the brain is directly connected to the rst pairof trunk ganglia via circumesophageal connectives. The four-

paired ventral ganglia do not show segmental commissurestypical of the ladder-like nervous system of euarthropods, butinstead represent a character state resembling the conditionof priapulids, kinorhynchs and nematodes where, apart from

Node (9) shows the Nematomorpha which, due to a para-sitic lifestyle, preserved a typical set of cephalorhynch char-acters, including a three-layered chitin-containing cuticleand a septum separating the introvert and abdomen, at thelarval and juvenile stages only. In adults, circular muscu-lature and the respiratory and circulatory systems are com-

pletely reduced, and the digestive and excretory (protone-phridia) systems are degenerated, while reproductive organsare hypertrophied; the body cavity is lled with a spacious

parenchyme; the two-layered cuticle of adult forms is builtof spiral collagenous bers and lacks chitin; and the nervoussystem comprises, in addition to the ventral nerve cord, anectodermal dorsal one (Nielsen, 2001, 2003). It is difcultto exclude the possibility that the horsehair worms reca-

pitulate some features of stem-lineage cephalorhynchs, suchas an annulated cuticle and a slim vermiform body lackinga distinct proboscis, a neck and an abdomen. Analyses of18S rRNA and histone 3 sequences indicate a sister-grouprelationship between loriciferans and nematomorths, which

might have evolved through progenesis (sexual maturationof larva) (Park, 2006; Srensen et al., 2008). This idea issupported by some morphological features of the larva andof the pharynx including a hexaradial arrangement of epithe-lial muscle cells and a triradiate lumen enclosed in myoepi-thelium, albeit the pharynx similarity can be a convergence(Nielsen, 2001; Srensen et al., 2008).

Node (10) crowns the vermiform ecdysozoan branch withthe Nematoda characterized by a low number of cells (eu-tely); a mostly collagenous cuticle, except for a pharyngealarea; and an absence of a proboscis even at the larval stages.The morphological similarity of the adult Nematomorpha to

the Nematoda, including hexagonal symmetry of cephalicstructures, can be interpreted as a heterochronic shift to thelatter group, reducing their possible nematomorph-like juve-nile stages and thus supporting the Nematoida clade (Zrzav,2001; Srensen et al., 2008). This suggestion has some sup-

port from molecular data (Bleidorn et al., 2002). Sometimesroundworms are cited as an example of organisation thatrejects the Ecdysozoa hypothesis due to the impossibilityof reaching such a simplication from a relatively complexancestor which possessed appendages, segmentation, andexcretory and nervous systems (e.g., Fitch, 2005). However,nodes (1) to (10) reveal that such a degeneration of the body

plan was achieved step by step in a very long row of nema-

tode ancestors.Node (11) places the Tardigrada acquiring: tagmosis;dorsal and ventral sclerotized plates and anges; non-meta-meric nephridia of a reduced number; suppression of circular

body-wall musculature; muscles in bundles, with each leghaving a different compliment of muscles; and segmentedganglia lacking commissures in the nerve cord (Dewel andDewel, 1997; Kristensen, 2002; Zantke et al., 2008; Edge-combe, 2009). Although some of these features resemblethose of the Euarthropoda, they probably were obtained con-

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ies are randomly scattered throughout the entire length ofeach nerve cord, resembling the organization in nematodesand platyhelminthes (Mayer and Harsch, 2007). Besides,velvet worms preserve a primitive neuroanatomy of their

pre-oral appendages (antennae), which are innervated by theprotocerebrum (Eriksson et al., 2003), while rst append-

ages of all living euarthropods are deutrocerebral. Ontogenicstudies indicate: that the onychophoran ventral mouth is em-

bryologically terminal (Eriksson et al., 2003); that the anten-nae are modied legs retaining the original arrangement oftransient nephridia anlagen at their bases despite the evolu-tionary change in position and function of these appendages(Mayer and Koch, 2005); and that the embryonic jaws andthe slime papillae are lobopod-like outgrowths (Strausfeldet al., 2006). The jaws in adult onychophorans are structureslike terminal claws of walking lobopods and thus can bederivates of lobopod terminal claws of ancestral xenusians.Budd (2001a) even suggested that onychophorans, as wellas tardigrades, and perhaps pentastomids, are merely extant

representatives of paraphyletic xenusians.Node (14) indicates the position of the Euarthropoda

(excluding the Tardigrada, the Onychophora and Pycno-gonida), which are characterized by: sclerotization; dis-tinct tergites; jointed segments and appendages; signicantcephalization expressed in a distinct head tagma anteriorlysubdivided into three elements, namely a protocerebral orocular region also bearing a labrum and a mouth, deutro-cerebral or antennal (cheliceral) region, and tritocerebral orsecond antennal (pedipalpal) region; biramous post-antennalappendages comprising an endopod and an exopod; a leversystem of muscles and a reduction of peripheral muscula-

ture; segmented bilaterally arranged ganglia that are longi-tudinally linked by connectives and transversely connectedby commissures in the ladder-like nervous system; saccu-late nephridia; and compound eyes. The latter show neithermorphogenetic nor ultrastructural similarities with those ofonychophorans (Mayer, 2006). On the contrary, the patternof someHox gene expression in onychophorans supports theidea that the development of arthropod joint limbs is derived

lateral commissures, none connecting the midventral nervecords have been reported.

In aggregate molecular studies using mostly EST data(Roeding et al., 2007; Dunn et al., 2008), and statisticallywell supported phylogenies grouping the Tardigrada with the

Nematoida (Lartillot and Philippe, 2008), together with ana-

tomical and morphological evidence, reveal that water bearshardly can represent an arthropod stem-lineage. Tardigradesmight originate from xenusians via Hadranax-type forms

possessing a heteronomous annulation (Budd, 2001b). It isnoteworthy that a Middle Cambrian fossil tardigrade fromSiberia bears cuticular plates (Maas and Waloszek, 2001,g. 9B) resembling those of some palaeoscolecidans (Pi-loscolex in Ivantsov and Zhuravlev, 2005, pl. XXI, g. 1).

Node (12) depicts the Kinorhyncha as a derivation of theTardigrada, thus revealing possible polyphyly for the Cepha-lorhyncha clade. Indeed, the kinorhynch autapomorphies in-clude metamery, enclosing of the integument, musculatureand nervous systems, sensory papillae, sclerotized dorsal

and ventral plates, and a retractable mouth cone equippedwith stylets (Nielsen, 2001; Neuhaus and Higgins, 2002),which equally can be treated as tardigrade/kinorhynch syn-apomorphies. On the other hand, it could have been scleroti-zation that led to transformation of the circular-longitudinalmuscle system into serially arranged dorso-ventral and di-agonal bunches and to segmentation of the nervous system.

Node (13) features Onychophora autapomorphies ofwhich there are: tagmosis; a ventral mouth, specialized an-tennae, jaws, slime papillae; segmented, diagonally oriented,leg muscles; an open circulatory system formed by fusionof both the coelomic cavities and the primary body cavity

into a haemocoel; segmented nephridia with functional cilia;and a dorsal heart with characteristic openings (ostia) intothe circulatory system (Nielsen, 2001; Eriksson et al., 2003;Edgecombe, 2009). Unlike the Euarthropoda, the bilaterally

paired ventral nerve cords are longitudinal structures con-nected to each other by numerous commissures but lackingsegmental thickenings as well as any recognisable serial orsegmental organization of neuron cell bodies; such cell bod-

tex-gue 5. General phylogeny of the Ecdysozoa. 0migration slag of amoebozoanDictyostelium discoideum Raper, extant; 1Urbilat-erian, hypothetic (modied from van Beneden, 1891); 2axenusianMicrodictyonsinicum Chen, Hou and Lu, Lower Cambrian (modiedfrom Hou and Bergstrm, 1995); 2xenusian Facivermis yunnanicus Hou and Chen, Lower Cambrian (modied from Delle Cave andSimonetta, 1991); 3Fieldia lanceolata Walcott, Middle Cambrian (modied from Conway Morris, 1977); 4Ancalagon minorWalcott,

Middle Cambrian (modied from Conway Morris, 1977); 5palaeoscolecid Cricocosmia jinningensis Hou and Sun, Lower Cambrian (modi-ed from Han et al., 2007); 6Louisella pedunculata Walcott, Middle Cambrian (modied from Conway Morris, 1977); 7priapulid larvaHalicryptus spinulosus von Seibold, extant (modied from Malakhov and Adrianov, 1995); 8loriciferan larvaPliciloricus ornatus Higginsand Kristensen, extant (modied from Malakhov and Adrianov, 1995); 9nematomorph larva Gordionus senkovi Malakhov and Spiridonov,extant (modied from Malakhov and Adrianov, 1995); 10nematodes Greefella (left) and Criconema (right), extant (modied from Bruscaand Brusca, 2003); 11tardigrade Stygarctus abornatus McKirdy, Schmidt and McGinty-Bayly, extant (modied from McKirdy et al., 1976);12kinorhynch Centroderes eisigii Zelinka, extant (modied from Malakhov and Adrianov, 1995); 13onychophoranPeripatopsis moseleyi(Wood-Mason), extant (modied from Ruhberg in Monge-Njera and Hou, 1999); 14larval euarthropodAscalaphus sp., extant; 15larval

pentastomidBoeckelericambria pelturae Walossek and Mller, Upper Cambrian (modied from Maas and Waloszek, 2001); 16anomalo-carididAnomalocaris saron Hou, Bergstrm and Ahlberg, Lower Cambrian (modied from Hou et al., 1995); 17protonymphon larva of

pycnogonidAnoplodactylus sp., extant (modied from Maxmen et al., 2005).

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plate-like teeth; ventro-lateral, stalked, compound eyes; ven-trally pointed, imbricating lobes, possibly with gill blades;and a tail fan (in the majority of forms) (Bergstrm, 1987;Hou et al., 1995, 2006; Daley et al., 2009). Budd and Telford(2009) added to this list midgut diverticulae and suggestedthat all the above-mentioned characters are synapomorphies

of the Euarthropoda. However, midgut diverticulae are pres-ent in vermiform ecdysozoans and xenusians, and thus repre-sent a symplesiomorphic feature, while the pre-oral positionof the only pair of jointed appendages can hardly be con-sidered an anomalocaridid-euarthropod synapomorphy. Onthe contrary, the mouth cone structure is completely incon-sistent with the euarthropod ground plan while pivot-joint

pre-oral appendages, compound eyes and a frontal carapace,which is developed inHurdia, rather resulted from a conver-gence due to a sclerotization of the cuticle at the head region.Even within the Euarthropoda, compound eyes may noteven be phylogenetically homologous to each other as the

same developmental programme allows for multiple originsof these organs through regulatory gene mutations (Oakleyet al., 2007). Certainly, euarthropod-type features were notaccumulated within the anomalocaridid lineage but merelydisplay a mosaic pattern acquired by them in a different tem-

poral order (e.g., Cucumericrus possesses appendages inter-mediate between lobopods and arthropodia and an abdomencovered by wrinkled skin rather than by tergites; Bergstrmand Hou, 2003). From a biomechanical point of view, pad-dle-like, lateral, overlapping lobes, plexus on lateral sides,skin-like cuticle, and large ventro-lateral eyes evident atleast inAnomalocaris andAmplectobelua are a logic conse-quence of pursuing swimming ability, if their lobes operated

as a continuous single ap, which is optimal for swimmingmotion as in a manta ray (Usami, 2006). Thus, the originof anomalocaridids is rooted in Kerygmachela-like swim-ming xenusians and in Tamisiocaris-like anomalocaridids

possessing unsclerotized soft appendages (Daley and Peel,2010). Another xenusian,Magadictyon cf. haikouensis, alsoaccumulated a number of anomalocaridid features including

Peytoia-like antero-ventral mouth cone with three circlesof cuneiform plates, and frontal appendages with terminalspines (Liu et al., 2007).

Possible offspring of the anomalocaridids are the Vetuli-colida, which are not indicated in Text-gure 5. These Cam-

brian animals were interpreted as early deuterostomes dueto the presence of gill pouches (Shu et al., 2001; Aldridgeet al., 2007). However, vetulicolians resemble stem-lineageecdysozoans by displaying: a segmented cuticularized body;a terminal mouth with a mouth cone consisting of 25 plates;and a straight alimentary canal with a terminal anus. Thisset of features including priapulid-type symmetry closelymatches that of ecdysozoans. In turn, so-called gill pouchescan be interpreted as midgut diverticulae like those found inthe Middle Cambrian arthropod Leanchoiliasuperlata and

from mechanisms present in this group (Panganiban et al.,1997), while a biramous limb comprising an endopod and anexopod evolved as a result of a split of the initial limb budwithin euarthropods (Wolff and Scholtz, 2008). The later hy-

pothesis is now supported by redescription of the Early Cam-brian primitive arthropodFuxianhuia, which lacks a special-

ization between and within ventral appendages (Chen et al.,1995; Bergstrm et al., 2009). Some other, mostly Cambrian,stem-lineage arthropods possibly possessed a pair of proto-cerebral sensory organs, known as frontal appendages orprimary antennae, in front of the deutrocerebral appendage

pair; thus a rotation of the anterior end of the body is impliedto obtain the present euarthropod ground plan (Scholz andEdgecombe, 2006; Hughes et al., 2008). Indeed, based on

joint study ofHox gene expression in embryologic develop-ment and of ontogeny, the euarthropod labrum is suggestedto be derived evolutionarily from paired limb-bud-like pri-mordia by rotation and fusion; this process is recapitulated

ontogenetically to a different extent in different arthropods;the labrum of at least arachnids and hexapods includes rem-nants of these ancestral appendages (Kimm and Prpic, 2006;Scholz and Edgecombe, 2006). The frontal appendagesthemselves were fairly simple limbs that could conceivablyevolve in various directions.

The placement of Node (15), the Pentastomida, is en-tirely based on molecular and spermatological analyses ac-cording to which pentastomids are highly derived parasitic

branchiuran crustaceans (Lavrov et al., 2004). However, aconvergence of spermatological features is thought to bewidespread among invertebrates, especially among parasites(Zrzav, 2001), while a more recent treatment of pentasto-

mid morphological characters indicates a position of pentas-tomids within the tardigrade/vermiform ecdysozoan clade(Almeida et al., 2008). In striking contrast to extant pentas-tomid larvae, late Cambrian fossils have a frontally placedmouth, two pairs of vestigial anterior appendages and up totwo pairs of rudimentary limbs on the tail part that are inter-mediate between a lobopod with claw-like terminations anda multi-segmented arthropodium of more advanced euar-thropods (Maas and Waloszek, 2001; Waloszek et al., 2006).Similarity of pentastomid claws with those of tardigradeswas noted by von Haffner (1977). At the same time, thesethree-dimensionally preserved larvae already demonstrate a

high degree of adaptation to parasitism. Thus, a direct root-ing of pentastomids within the Xenusia cannot be excludedat the moment (but see Lavrov et al., 2004, who excludeCambrian putative pentastomids from tongue worms). The

pentastomid autapomorphies include an unusual cuticular-chitin and a suctorial mouth anked by two pairs of hooks.

Node (16) points to the most unusual ecdysozoan stem-lineage, the Anomalocaridida, autapomorphies of whichinclude: sclerotized and articulated pre-oral grasping ap-

pendages; an antero-ventral mouth cone with a circlet of

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intermediate forms, supporting the Articulata hypothesis, thusrejecting the critics of the Ecdysozoa concept. Highly vari-able morphologically xenusians, which crawled with theirlobopods along the sediment surface, may have given riseto four morphofunctional lineages, namely to: stem-lineagecephalorhynchs (via Facivermis-type forms) by adaptation

for burrowing with introvert; tardigrades (viaHadranax-likeforms) by adaptation for an interstitial habitat; stem-lineage

panarthropods (viaLuolishania-type forms) by adaptation toa walking lifestyle with joint appendages; and anomalocari-dids (viaKerygmachela-type forms) by adaptation to swim-ming with lateral aps in the pelagic realm. The nds of suchforms as Pambdelurion with diagonal muscles, Paucipodiawith structures resembling paired ventral ganglia, Jiansha-nopodia with a some kind of biramous appendages bearing aapping exopod, andLuolishania with advanced cephaliza-tion (Budd, 1998; Hou et al., 2004b; Liu et al., 2006b; Maet al., 2009) may indicate that even the euarthropod ground

plan can be developed independently, as all these features areabsent in onychophorans. Besides, neither a ventral mouth,nor antennae, nor, probably, eyes in onychophorans are ho-mologous to those structures in euarthropods. However,many attempts to create an euarthropod creature on the xenu-sian body ground

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