the early history of the metazoa—a paleontologist’s … brachiopods are not intermediate between...

ISSN 2079�0864, Biology Bulletin Reviews, 2015, Vol. 5, No. 5, pp. 415–461. © Pleiades Publishing, Ltd., 2015.Original Russian Text © A.Yu. Zhuravlev, 2014, published in Zhurnal Obshchei Biologii, 2014, Vol. 75, No. 6, pp. 411–465.

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INTRODUCTION

When Charles Doolittle Walcott discovered the firstLagerstätte (from the German Lager “storage,”Stätte� “place”) 100 years ago—the Burgess Shale inwestern Canada—everything seemed relatively sim�ple: wormlike organisms were interpreted as annelidworms, organisms with segmented limbs as arthro�pods, and rounded imprints with radial lobes wereinterpreted as jellyfish (Walcott, 1911a, 1911b, 1912).At the end of the 1970s, old collections from the Bur�gess Shale were reexamined, more samples were col�lected, and new Lagerstätten were discovered. Theseinclude Chengjiang in South China, Sirius Passet For�mation, northern Greenland, Sinsk Lagerstätten inCentral Yakutia, Emu Bay Shale in South Australia,and the Middle Cambrian Lagerstätten of Murero,Aragón in northeastern Spain, which yielded many ofthe most interesting fossils. At the same time it hasbecome clear that the most interesting specimens didnot fit into the classical concepts of the comparativeanatomy of the ancestral bauplan. These have beenrecognized, sometimes based on a few specimens, as

representatives of separate, long extinct phyla. Gould(1989), best known for the theory of “punctuatedequilibrium,” was particularly supportive of thisapproach, which suggested that fossils like Opabiniawith five faceted eyes, lobes (flaps), and a segmentedproboscis or Hallucigenia with paired spines instead oflimbs and flexible unpaired limbs along the back, arein fact artefacts of ancient Metazoa: they are not stemgroups to extant phyla, but taxa that competed withthem for resources in the Early Paleozoic and ulti�mately lost.

At the same time, molecular biologists, based oncomparative analysis of homologous DNA nucleotidesequences and a comparison of the order of expressionof homeobox complexes, and later the comparison ofcomplete genomes, began to challenge the postulatesof classical comparative anatomy. Their studies haveshown that arthropods are not related to annelids but,together with priapulids and nematodes, form theclade Ecdysozoa (periodically molting animals);whereas brachiopods are not intermediate between theprotostome and deuterostome animals but, togetherwith annelids, mollusks, bryozoans and other tenta�

The Early History of the Metazoa—a Paleontologist’s ViewpointA. Yu. Zhuravlev

Geological Institute, Russian Academy of Sciences, per. Pyzhevsky 7, Moscow, 7119017 Russiae�mail: [email protected] January 21, 2014

Abstract—Successful molecular biology, which led to the revision of fundamental views on the relationshipsand evolutionary pathways of major groups (“phyla”) of multicellular animals, has been much more appre�ciated by paleontologists than by zoologists. This is not surprising, because it is the fossil record that providesevidence for the hypotheses of molecular biology. The fossil record suggests that the different “phyla” nowunited in the Ecdysozoa, which comprises arthropods, onychophorans, tardigrades, priapulids, and nemato�morphs, include a number of transitional forms that became extinct in the early Palaeozoic. The morphologyof these organisms agrees entirely with that of the hypothetical ancestral forms reconstructed based on onto�genetic studies. No intermediates, even tentative ones, between arthropods and annelids are found in the fos�sil record. The study of the earliest Deuterostomia, the only branch of the Bilateria agreed on by all biologicaldisciplines, gives insight into their early evolutionary history, suggesting the existence of motile bilaterallysymmetrical forms at the dawn of chordates, hemichordates, and echinoderms. Interpretation of the earlyhistory of the Lophotrochozoa is even more difficult because, in contrast to other bilaterians, their oldest fos�sils are preserved only as mineralized skeletons. However, the unity of the microstructures of mollusks, bra�chiopods, and bryozoans, which is absent in other metazoans, is indicative of the presence of close relativesamong the various earliest lophotrochozoans, some of which were sedentary suspension�feeders while otherswere mobile epibenthic detritophages. In the aggregate, modern data from molecular biology, palaeontology,and comparative embryology/morphology, having been revitalized by the introduction of new microscopytechniques, imply that the hypothesized planktotrophic gastrae�like common ancestor is the least likely of thediverse suggestions on the origins of the Metazoa. The common ancestor of the Bilateria had to be a motileepibenthic animal, and the explosive metazoan diversification embracing the Late Ediacaran–Early Cam�brian interval (c. 40 Ma) was probably a real event, which was predated by a long (ca. a billion years) periodof the assembly of the metazoan genome within the unicellular and colonial common ancestors of theOpisthokonta, and possibly even the entire Unikonta.

DOI: 10.1134/S2079086415050084

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cled animals, form another big clade, Lophotro�chozoa (Halanych et al., 1995; Aguinaldo et al., 1997;Aleshin et al., 1998). Only Deuterostomia haveremained as an unshakable bastion of comparativeanatomy, although it included the enigmatic taxonXenoturbella, once placed among flat worms. At first itseemed like a revolution that had failed to materialize,a game based on large numbers of unsubstantiatedcharacters (Wägele and Misof, 2001; Nielsen, 2003;Philip et al., 2005). However, as time passed, theseseemingly eccentric theories did not fade but insteadbecame more clearly outlined (Baguñà et al., 2008;Colgan et al., 2008; Helmkampf et al., 2008; Hejnolet al., 2009; Paps et al., 2009; Braband et al., 2010;Ogino et al., 2010; Edgecombe et al., 2011; Telfordand Copley, 2011). Moreover, the ideas of molecularbiologists were met with genuine interest and sup�ported by the (literally) rock�hard evidence providedby paleontologists studying the morphology of Cam�brian fossils.

Success in molecular biology outlined new param�eters of phylogenetic trees and allowed the correctplacement of the several problematic Cambriangroups (e.g., Palaeoscolecida, Xenusia, Anomalocari�didae) among Ecdysozoa, as well as diverse Cambrianobjects known as “small shelly fossils.” Only 10–15 years ago these 20–30 large groups (tommotiids,halkieriids, Hadimopanella and many others), whichcomprise a considerable proportion of Cambriandiversity, appeared never to have been confidentlyplaced anywhere in the phylogeny of Metazoa.

The Metazoan molecular trees are presently subdi�vided into the braches Porifera (Hyalospongia, Demo�spongia and Calcarea, and also Homoscleromorpha),Placozoa (Trichoplax), Cnidaria (including Myxo�zoa), Ctenophora, Acoelomorpha (nemertodermatidsand Acoela, sometimes with Xenoturbella), Deuteros�tomia (echinoderma, hemichordates and chordates,sometimes together with Xenoturbella), Chaetog�natha, Ecdysozoa (nematodes, Nematomorpha, Pri�apulida, Loricifera, Kinorhyncha, Tardigrada, Ony�chophora, Arthropoda, including Pentastomida),Lophotrochozoa (Bryozoa, Kamptozoa, Cyclio�phora, Orthonectida, Brachiopoda, Phoronida, Mol�lusca, Nemertea and Annelida, including Myzosto�mida, Echiurida, Sipunculida and Pogonophora / Ves�

timentifera, and also Rhombozoa) and Platyzoa(other Platyhelminthes, Gastrotricha, Acanthoceph�ala, Micrognathozoa, and Rotifera); Lophotrochozoaand Platyzoa are sometimes assigned together to Spi�ralia (Passamaneck and Halanych, 2006; Bleidornet al., 2007; Jiménez�Guri et al., 2007; Sperling et al.,2007; Dunn et al., 2008; Jenner and Littlewood, 2008;Marlétaz et al., 2008; Struck and Fisse, 2008;Yokobori et al., 2008; Egger et al., 2009; Struck et al.,2011 above papers). Based on purely molecular data,the position of some organisms (Xenoturbella) and thecomposition of some groups (Acoelomorpha,Platyzoa) remain debatable: Xenoturbella, e.g., areassigned together with Acoelomorpha to Deuterosto�mia (Philippe et al., 2011; Nakano et al., 2013) (Fig. 1).The relationships of some units within the Ecdysozoa,Lophotrochozoa and Deuterostomia, are still unre�solved. However, the multiplication of sequencedgenes and species allows the determination in each ofthese groups of a suitable place for previous phyla thatbetter agrees with concepts of comparative anatomy.For example, data on 196 genes for 58 species ofLophotrochozoa revealed that Bryozoa, Phoronida,and Brachiopoda are sister groups within the Lopho�phorata and established sister�group relationshipsbetween Lophophorata and Kamptozoa+Cycliophora(Nesnidal et al., 2013), whereas previous insufficientsampling had united brachiopods, phoronids, andnemerteans in the bizarre group Kryptrochozoa(Dunn et al., 2008; Giribet et al., 2009).

The problem of the basal groups—sponges, cni�darians, Trichoplax, and triploblastic ctenophores—remains a tangled knot in the evolution of Metazoa.After the discovery of Homoscleromorpha were previ�ously considered a family and suborder in the classDemospongiae with a basal membrane consisting ofcollagen IV and laminine underlining the choano� andpinacoderm and ciliate epithelium in the cincto�blastula. Homoscleromorpha and spermatozoids withhacrosomes, i.e., characters unknown in othersponges but typical of triblastic Metazoa, were recog�nized as a separate class of sponges, and this assign�ment was supported by molecular data (Ereskovskyet al., 2009; Gazave et al., 2012). Working hypotheseson the succession of appearances and relationships ofvarious sponges, cnidarians, ctenophores, and Tri�choplax are very different and sometimes contradic�

Fig. 1. Molecular phylogeny of Unikonta after Edgecombe et al. (2011); Nesnidal et al. (2013); Nosenko et al. (2013); Sebé�Pedrés et al. (2013) with added paleontological data (only the earliest fossils representing different groups are shown). Top—radi�ometric scale in Myr (not to scale). The boundary of 540 Ma approximately corresponds to the Ediacaran–Cambrian boundary.Amoebozoa (lifecycle of the Ediacaran slime mold Gaojiashania), Annelida (Cambrian Burgessochaeta), Anomalocaridida(Cambrian Amplectobelua), Arthropoda (Cambrian Fuxianhuia), Brachiopoda (Cambrian Longtancunella, Chileata), Calcarea(Cambrian Eiffelia), Cephalochordata (CambrianYunnanozoon), Chaetognatha (Cambrian Protosagitta), Cnidaria (CambrianCtenorhabdotus), Demospongiae (Cambrian archaeocyath Coscinocyathus), Echinodermata (Cambrian Ctenoimbricata), Fungi(Cryogeniv fungus “Tappania”), Hemichordata (Cambrian Spartobranchus), Hexactinellida (Cambrian Protospongia), Kamp�tozoa (?Cambrian Cotyledion), Mollusca (Silurian Acaenoplax, Aplacophora + Polyplacophora), Palaeoscolecida (Cambrianpalaeoscolecid worm), Priapulida (Cambrian Yunnanpriapulus), Tommotiida (Cambrian Camenella), Vendobionta (lifecycle ofthe vendobiont Fractofusus + Charnia), Vetulicolia (Cambrian Vetulicola), Xenusia (Cambrian Microdictyon). © Artist VsevolodAbramov.


THE EARLY HISTORY OF THE METAZOA 417

1700

AmoebozaApusozoa

Nucleariidae

FungiVendobionta

IchthyosporeaFilasterea

ChoanoflagellataHexactinellidaDemospongiae

Calcarea

HomoscleromorphaCtenophora

PlacozoaCnidaria

Xenoturbellida

Nemertodermatida

AcoelaCephalochordata

Urochordata

CraniataEchinodermata

Hemichordata

ChaetognathaTardigrada

Anomalocaridida

OnychophoraXenisia

VetulicoliaLoricifera

PalaeoscolecidaNematomorpha

MolluscaAnnelida

Coeloscleritophora

BryozoaBrachiopoda

AmoebozoaCycliophora

Kamptoza

Gastrotricha

Tommotiida

Gnathostomulida

Micrognathozoa

Vendobionta

1000 550580 540

ArthropodaPriapulida

Kinorhyncha

Nematoda

Nemertea

Phoronida

Platyhelminthes

Rotifera

million years

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tory (Borchiellini et al., 2001; Malakhov, 2004, 2010;Wallberg et al., 2004; Schierwater et al., 2009; Picket al., 2010; Ryan et al., 2010; Martindale, 2013).Apparently, to catch the molecular signal of phyloge�netic branches that diverged early in phylogeny, a sim�ple accumulation of molecular data is insufficient,even when all of these data are based on the analysis oforthologs. It is essential to analyze the groups of genesthat most clearly show early branching in the evolutionof basal Metazoa, e.g., ribosomal genes (Pick et al.,2010; Philippe et al., 2011; Nosenko et al., 2013). Inaddition, it should be understood that all moderngroups in their evolutionary history passed through thebottlenecks of mass extinctions, which could severelydeplete their genetic diversity, e.g., as was observed inctenophores (Podar et al., 2001). Since the addition tothe molecular dataset of data from a single group ofMonoplacophora changes the entire architectonics ofmollusk molecular trees (see below), it seems unlikelythat molecular trees are sufficient on their own, with�out paleontological data, to resolve dozens of such keygroups.

SEDIMENTOLOGY AND TAPHONOMYAS A BASIS FOR MODERN PALEONTOLOGY

Before continuing with the next section, it is worthbearing in mind that the end of the Cryptozoic–begin�ning of the Phanerozoic eons/eonothems of the Inter�national Chronostratigraphic Scale is subdivided in tothe Cryogenic (850–635 Ma), Ediacaran (consideredto be equivalent to the Vendian in Russia) (635–541 Ma),Cambrian (541–485 Ma), and Ordovician (485–443 Ma)periods/systems (radiometric data of the absolute ageare in brackets). The Cambrian period/system untilrecently included three epochs/series: Early/Lower(541–509 Ma), Middle/Middle (509–495 Ma) andLate/Upper (495–485 Ma); this division is acceptedhere for simplicity. A distinct boundary between theeonothems, noted in the 19th century and drawn atthe base of the Cambrian system, is related to the massappearance of organisms with a mineral skeleton,leading to the subsequent formation of localities withabundant burials of “soft�bodied” animals.

The “soft�bodied” organisms are preserved in par�ticularly strictly defined environments which arereferred to as Lagerstätten. The Cambrian Lagerstättenare thin (composed of clay�size particles, ≤ 4 μm) sedi�mentary rocks usually of marine origin with limitedoxygen content. Organisms were carried to theseplaces by turbidity currents, underwater mudslides, orother fast events (Ivantsov et al., 2005; Caron andJackson, 2006; Gaines et al., 2012). The surface ofbeds with assemblages of such fossils organisms there�fore represent instantaneous casts of ancient events(rather than an averaged representation, as occurs inthe deposits that are accumulated in normal condi�tions during the rapid processing of organic matter byscavengers and decomposers), the dissolution of shells

lacking protective organic films, and the mixing of sea�floor sediment matrix by bioturbators (borrowing ani�mals), which results in situations in which a coquinabed only 1 cm thick can contain fossils that have accu�mulated over 15000 years. The low oxygen level in theCambrian basins (Saltzman, 2005; Gill et al., 2011)was an important condition for the formation ofLagerstätten, because it prevented activity of bioturba�tors. In the absence of bioturbators, organisms werepreserved in their entirety, rather than as disassembledsegments, spicules, or sclerites. In organisms with a rigidcuticle, the rate of mineralization of soft tissues (theirreplacement by clay minerals, silica, pyrite, or phos�phate) could be greater than their decomposition rate.

Therefore, the Cambrian Lagerstätten of the “Bur�gess type” primarily contain mineralized casts of rela�tively large animals with a developed cuticle. Of these,cuticular remains of Ecdysozoa as isolated larval skinsor, less commonly, casts of organisms with some min�eralized soft tissues constitute 70% or more of the totalnumber of species and individual organisms in the fos�sil assemblage and of its total biovolume (in paleoecol�ogy this parameter is used instead of the biomass)(Conway Morris, 1986; Ivantsov et al., 2005; Caronand Jackson, 2006; Dornbos and Chen, 2008; Zhaoet al., 2013). The “taphonomic window” (the intervalwith the most Cambrian Lagerstätten) opened whenEcdysozoa acquired rigid cuticles and closed when theoxygen levels in relatively deep marine basinsincreased, facilitating bioturbators, which in turnincreased aeration of the sediment. The CambrianEcdysozoa include Arthropoda, Cephalorhyncha, andexinct groups (classes or stem groups using cladisticterminology), i.e., Xenusia (with a wormlike annu�lated body, lobopodian retractile legs, and a long pro�boscis), Anomalocarididae (with compound stalkedeyes, segmented grasping appendages in front of themouth, triradiate oral cone possessing plates, andswimming lobes) and, perhaps, Vetulicolia (Hou andBergstrom, 1995; Budd, 1998; Hou et al., 2006; Maet al., 2009; Harvey et al., 2010; Gámez Vintanedet al., 2011; Zhuravlev et al., 2011b) (Fig. 2). Cha�etognatha, Hemichordata, and Chordata with a rela�tively thick epithelium (Shu et al., 2003b; Chen andHuang, 2002; Caron et al., 2013a), Cnidaria with chi�tinized tubes, and Ctenophora (Conway Morris andCollins, 1996; Hou et al., 1999) constitute another 5%.The remaining 25% are represented by sponges, echi�noderms, mollusks, annelids, and the Lophotro�chozoa, the preservation of which in Lagerstätten dif�fers from that in normal deposits only in that theirskeletal elements, including nonmineralized ele�ments, remain in a lifelike position. Brachiopods,mollusks and annelids rarely have primary chitinouschaetae, or during phosphatization, imprints of cells,even of microvilli on the shell surface (Ushatinskayaand Parkhaev, 2005). In addition, in the remains ofbrachiopods and other tentacled animals with stronglychitinized covers, it is sometimes possible to discern a



pedicle, digestive tract, and lophophore with ciliatedtentacles (Zhang et al., 2004, 2009). It is possible toestimate other ecological parameters, e.g., speciesdiversity or abundance, with the same total result:Ecdysozoa is the overall dominant group (Zhao et al.,2013). In other types of occurrences, molluskan “bod�ies” are preserved in extreme circumstances, e.g., inthe Silurian Herefordshire Lagerstät (425 Ma), wherethey were preserved as calcite in�fills within nodulesentombed in an ancient volcanic ash (Sutton et al.,2001, 2012).

The Örsten�type Lagerstätten, named after thetype Late Cambrian locality in Sweden, in contrast tothe Burgess�type, contain only small phosphatized

remains, including embryos, larvae, and fragments oflarge organisms, all of which except in extremely rareinstances, belong to Ecdysozoa (Müller, 1979; Maas etal., 2006). The phosphatized embryos, which shouldbe arranged in successions from the initial stages ofcleavage to gastrulation and the development of theadult organism, are sometimes assigned to cteno�phores, cnidarians, and some inserta sedis groups,such as Pseudooides, whereas Lophotrochozoa areabsent (Bengtson and Yue, 1997; Kouchinsky et al.,1999; Chen et al., 2007), although the Ecdysozoaaffinity of some embryos of “Cnidaria” or “Cteno�phora” cannot be completely excluded (Liu et al.,2014; Steiner et al., 2014).

b

c

edf

h g

i

j

a

Fig. 2. Cambrian Ecdysozoa: (a) paleoscolecid worm, (b–f) Xenusia: (b) Mureropodia, (c) Microdictyon, (d) Diania, (e) Anten�nacanthopodia, (f) Pambdelurion, (g–j) Anomalocaridida: (g) Amplectobelua, (h) Nectocaris, (i) Hurdia, (j) Vetulicola. The ani�mal reconstructions are modified after Budd (1998); Hou et al. (1999); Aldridge et al. (2007); Daley et al. (2009); Smith andCaron (2010); Gamez Vintaned et al. (2011); Liu et al. (2011); Ou et al. (2011); Zhuravlev et al. (2011b); Ma et al. (2014).© Artist Vsevolod Abramov.

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Orsten�type Lagerstäten are mostly found in theEdiacaran and Cambrian beds and were probablyformed when anoxic water masses upwelled into theshallow shelf or resulted from intense hydrothermalactivity (Donoghue et al., 2006; Yin et al., 2014). Thebest�known Ediacaran Lagerstät of this type is a Dous�hantuo phosphorite Lagerstätte, in Guizhou, SouthChina, in the thick phosphotite Weng’an member(630–620 Ma). This locality contains giant acritarchs,algae, presumed embryos, sponges, corals, and theearliest Bilateria (Vernanimalcula) with a circulatorysystem, paired coelomes, gut, etc. (Li et al., 1998;Chen et al., 2004; Liu et al., 2008). Bengtson et al.(2012) published a particularly high impact paper onVernanimalcula, in which they calculated that theoriginal article by Chen et al. (2004a) has attractedmore than 160 citations, including publications on theorigin of bilateral symmetry, the circulatory system,eyes, and even cancer. However, the paper by Bengt�son et al. (2012), entitled (with reason) “A MercifulDeath for the ‘Earliest Bilaterian,’ Vernanimalcula”concluded, based on the study of fibronormal crystalsof the apatite minerals forming this fossil, that all “lay�ered tissues” and “organs” were the effects of mineral�ization of phosphatized layers formed at various stagesof diagenetic (secondary abiogenic) modification oforganic matter of uncertain origin possessing micro�scopic cracks. The so�called spiculate sponges fromthe Weng’an phosphorite are likewise of inorganicnature: neither the microstructure, nor chemical com�position of micrometer�sized acicular structures pro�vide substantial evidence for their assignment tosponge spicules (Yin et al., 2001). The structures inter�preted as “corals,” in light of their microscopic size(diameter less than 100 μm), very regular dichotomousbranching and arrangement of tabulae, as well as thelack of partitions, are renalcids—organisms of uncer�tain affinity resembling some algae from the groupsViridiplantae and Rhizaria that were common in theEdiacaran�Cambrian (Liu et al., 2010; Zhuravlevet al., 2011a).

Phosphatized embryos were also difficult to inter�pret. The so�called embryos were spherical microfos�sils (on average 300–650 μm across) with a distinctpolygonal ornamentation composed of smallerspheres (Xiao et al., 1998). However, the same appear�ance is observed in cysts of Holozoa (Protista) (Huldt�gren et al., 2011), Viridiplantae, and giant sulfur bac�teria (Bailey et al., 2007), and even layers of diageneticphosphate mineral (Bengtson and Budd, 2004). Min�eralogical study of these microfossils and their chemi�cal element composition (C, Ca, P, and F) showed thatthe multiple layers cannot be interpreted as originalcellular layers; they were mainly formed in late diagen�esis, thereby excluding the possibility of interpretingthese structures as colonial bacteria or embryos such asgastrulae (Cunningham et al., 2012a, 2012b). Imagingtechniques using propagation phase�contrast basedsynchrotron radiation microtomography of some

Weng’an fossils showed that irregularly elliptical32�cell stage objects resemble embryos with a visiblemicromere cap at one end and macromeres arrangedin a row at the opposite end, nearer the “ventral side.”In gastrulae such a row precedes the development ofthe gust, whereas micromeres give rise to integumentcells (Chen et al., 2009; Yin et al., 2013, 2014). It mustbe noted that, among the millions of phosphatizedmicrofossils, multiple objects with similar shape orcomplexity can be found, like finding a pebble strik�ingly similar to a chicken bone on a large beach. Thus,the Doushantuo phosporites suggest so far that multi�cellular algae (Viridiplantae or Stramenopiles) existedat the beginning of the Ediacaran period (which, infact, appeared earlier, see Butterfeld, 2009)—possiblyeven in simple embryos in the early stages of splitting.

As for the Cambrian Lagerstätten, it should be saidthat the dominance of Ecdysozoa in all these assem�blages is related not only to good preservation of theirinteguments but also to the geochemistry of the Edi�acaran–Cambrian oceans, which still retained fea�tures of the stratified Canfield Ocean (Canfield, 1998).The deep layers of this ocean were largely euxinic toanoxic (which spread to shallow waters during regres�sions), which was concluded based on sedimentologi�cal, mineralogical, and isotope analysis (34S/32S,13C/12C) and the increased content of Mo, U, and V(Li et al., 2010; Gill et al., 2011; Pi et al., 2013). SomeEcdysozoa are adapted to such conditions. AmongLoricifera, there are obligatory anaerobic taxa surviv�ing anoxic conditions due to hydrogenosome�likeorganelles (Danovaro et al., 2010), while priapulidsand nematodes can live through long periods of anoxia(Oeschger, 1990; Vanreusel et al., 2010). Analysis ofthe deepest water Cambrian assemblages (sublittoral)shows that they included species with different adap�tations to life in an oxygen�depleted environment(Ivantsov et al., 2005).

This taphonomic background was necessary,because the appearance of the ancient organisms andtheir role in the paleocommunities are largely judgedfrom the analysis of Lagerstätten. Such an analysis isimpossible without a basic knowledge of sedimentol�ogy (study of the processes of formation of sedimen�tary deposits) and taphonomy (study of transforma�tion of dead organisms into fossils). These fields serveas the basis for modern paleontology. From the view�point of taphonomy, conclusions recently published inprestigious journals by Smith and Caron (2010) andSmith (2013), seem insufficiently substantiated. Thesepublications address the occurrence in the Cambrianrocks of numerous samples with imprints of the soft�bodied cephalopod Nectocaris pteryx (this organismwas previously interpreted as belonging to Arthropodaor Chordata) (Fig. 2h). The probable existence of suchan ancient cephalopod, which, as reconstructed bySmith and Caron (2010) and Smith (2013), had pairedcamera�like eyes on short stalks, lateral fins, well�developed gills, and a funnel (hyponome) suitable for



jet propulsion, revolutionized the interpretation of theearly evolution of cephalopods. Until recently it wasbelieved, based on paleontological evidence, that thecoleoid cephalopods in the Devonian Period (ca. 400 Ma)had evolved from cephalopods with an external shell,which originated in the Cambrian from some kind ofmonoplacophorans or gastropods. These old recon�structions need to be fundamentally critically revised.It is not surprising that malacologists were skepticalabout the above interpretation. They noted that theanimal could not have had a gut if the axial cavityclearly visible in the fossil imprints was a mantle cavity.However, if that was a gut, then the structures in itcould not have been gills; the hyponome lacked a cir�cular mantle muscle and widened distally and thus wasunlikely to be suitable for jet propulsion; and there wasonly one pair of frontal tentacle�like appendages(Kröger et al., 2011; Mazurek and Zato �n, 2011; Run�negar, 2011). The presence of one hundred molluskspecimens (if Nectocaris is interpreted as a mollusk)lacking a shell is doubtful in itself. Smith (2013) indi�cated that the covers of this fossil, which were replacedby the clay mineral chlorite, has an elevated calciumconcentration. Chlorite of such composition is formedwhen clay minerals replace originally strongly miner�alized tissues of the calcareous skeleton (Zhuravlev etal., 2011b). In Smith’s opinion the gills in Nectocariscould be phosphatized. However, the position of thiscomplex of organs along the axial cavity and theirprominence and phosphatic composition suggests thatthese were digestive diverticula (Butterfeld, 2002;Zhang and Briggs, 2007; Zhuravlev et al., 2011b).Conversely, gills in Cambrian argillaceous Lagerstät�ten are not phosphatized, while phosphatized gills arefound in Mesozoic anoxic marine deposits, but in thatcase other soft tissues are also phosphatized. Thereforethe axial cavity of Nectocaris is interpreted as a straightgut with a terminal anus and mouth at the end of the“hyponome,” which is adjacent to the gut. In this casethe “hyponome” is a proboscis, the tentacles arepaired mouthparts, and the coarse stripes along thefins are external gill filaments. This complex of organsis typical of anomalocaridids (Ecdysozoa) common inthe Cambrian Lagerstätten (Budd, 2001; Daley et al.,2009) (Figs. 2g and 2i). The presence of camera�likeeyes does not contradict this conclusion, as similareyes are found in Ecdysozoa, e.g., in extant arthropods(Land, 2005) and onychophorans (Mayer, 2006), andalso in Cambrian Xenusia (Schoenemann et al.,2009), which are close relatives of anomalocaridids.

A detailed analysis of Smith’s work was necessary,because neonatologists sometimes too quickly acceptthe conclusions derived from such publications. Ifthese papers are published in high�impact journals,they have every chance of a long life, and, as Bengtsonet al. correctly pointed out, a fairly “merciful death”may go unnoticed. This does not mean that paleonto�logical evidence cannot be trusted, but some interpre�tations of this evidence can be deeply erroneous.

THE TALE OF HOW MOLECULAR BIOLOGY MET PALEONTOLOGY,

WITH CONSEQUENCESFOR COMPARATIVE ANATOMY

Trichoplax and the Vendobionts

The study of the complete mitochondrial genomeof Trichoplax showed that it contains regions unique tothe Metazoa, and also includes introns similar to thoseof chytrid fungi and Choanoflagellata; this genome islarger than the mitochondrial genome of any otherMetazoa (43079 bp) due to large intragenic spacersand genes encoding proteins of unknown function(Dellaporta et al., 2006). Although the completegenome of this organism, which was later sequenced,was shown to be more complex than previouslythought, suggesting secondary loss and simplificationof the animal (Srivastava et al., 2008), Trichoplax wasaccepted as an ideal model of the basal stem organismfor all metazoan animals (Rozhnov, 2010; Sperlingand Vinther, 2010). The authors came to this conclu�sion after having studied Trichoplax and compared aseries of its feeding traces with those of Vendobionta.However, it is unlikely that the mode of locomotion ofa millimeter�size Trichoplax using flagellated cells ofthe ventral epithelium could be used by organisms thatwere larger by three orders of magnitude.

Seilacher (1989, 1992) coined the name Vendo�bionta for large (up to 1 m long or longer) Ediacaranfossils composed of segment�like units (frondlets),which, unlike true segments, can be arranged alongany axis of an organism and form a relief quilted sur�face (Figs 3a–3h). These fossils had previously beenplaced within the jellyfish, mollusks, annelids, echin�oderms, etc., although they resemble these animalsonly in artistic reconstructions (Glaessner, 1984; Jen�kins, 1992; Dzik, 2011). Authors occasionally do notnotice that the fossil animal assigned to Proarticulatadiffers from a cast interpreted as a diploblastic animalonly by a slightly less pronounced spiral arrangementof frondlets (e.g., Paravendia janae (Ivantsov, 2004)and Eoandromeda octobrachiata (Zhu et al., 2008))(Figs. 3g and 3h).

According to radiometric dating, Vendobionta arefound in beds 579–543 Ma in age (Martin et al., 2000;Lafamme et al., 2013). Fedonkin (1983, 1987) was thefirst to notice that many of these organisms have a sim�ilar type of segmentation and glide reflection symme�try (expressed as a half�step shift of the conditionallyleft frondlets in relation to the mirrored right frondletsalong the body axis) that is not observed in any Meta�zoa (Figs. 3b–3g). Such fossils are frequently inter�preted as ancient worms or arthropods. Apart from aparticular type of symmetry, the major groups of Ven�dobionta (Triradialomorpha (Fig. 3a), Rangeomorpha(Figs. 3b and 3c), Arboreomorpha (Fig. 3d), Petal�onamae (Fig. 3e), Proarticulata (Figs. 3f and 3g),Bilateralomorpha) are similar to one another and dif�ferent from Metazoa in the absence of a mouth, anus,

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gut, any kind of zooids and unlimited, not isometric,growth with terminal, including bipolar, asymmetricinsertion of new frondlets (Zhuravlev, 1993a; Grazh�dankin and Seilacher, 2002; Peterson et al., 2003; Ant�cliffe and Brasier, 2008; Naimark and Ivantsov, 2009).In addition, vendobionts are often preserved in largenumbers in coarse�grained sandstones, without losingdetails of their morphology, which is impossible evenfor organisms with a mineral skeleton. The coarser thesediment is, the more prominent is the morphology ofvendobionts. When the same species are buried in afine�grained sediment, they have on their surface arigid organic film present in the fungi and algae found

in the same beds (Grazhdankin and Seilacher, 2002;Grazhdankin, 2004; Zhu et al., 2008).

However, the largest difference is in the internalstructure of the organisms, in the presence of a systemof tube�like units chambers (vanes) that are subquad�rate in a cross�section and penetrating the entire body(the length of the chambers greater than the width byone–two orders of magnitude) (Petalonamae (Fig. 3e),Proarticulata (Fig. 3f), Bilateralomorpha) or thinbifurcating canals arranged in one plane (Rangeomor�pha (Figs. 3b, 3c, and 3j), Arboreomorpha (Fig. 3d)),which was revealed using high resolution laser scan�ning and digital mapping. It is this system of units thatgives vendobionts their quilt�like appearance (Xiao et

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Fig. 3. Ediacaran Vendobionta: (a) Tribrachidium (Triradialomorpha), (b, j) Beothukis (Rangeomorpha), (c) Fractofusus(Rangeomorpha), (d) Charniodiscus (Arboreomorpha), (e) Pteridinium (Petalonamae), (f) Dickinsonia (Proarticulata),(g) Paravendia (Proarticulata), (h) Eoandromeda, (i) Nilpenia. The reconstructions are modified after (2004); Serezhnikova(2007); Grazhdankin, Seilacher (2002); Brasier and Antcliffe (2008); Zhu et al. (2008); Brasier et al. (2012); Droser et al. (2014).© Artist Vsevolod Abramov.



al., 2005; Brasier and Antcliffe, 2008; Brasier et al.,2012). Both systems are of the closed type, i.e., they donot communicate with the outside environment byany kind of pores. The tube�like chambers contact oneanother along their entire length (Grazhdankin andSeilacher, 2002; Brasier and Antcliffe, 2008). Thecanals uniformly fill the entire body, including the“head” in Proarticulata and Bilateralomorpha(Ivantsov, 2004, text�figs. 4–6); as they approach thesurface, the canals bifurcate from three to five times,progressively decreasing in diameter, resulting in afractal pattern like Escher’s “Regular Division of thePlane.” In some Proarticulata, e.g., Dickinsonia, thesystem of tubes is combined with canals (Ivantsov,2004, pl. 1, fig. 7).

All of this suggests that vendobionts occupy a sepa�rate position among multicellular animals, i.e., thatthey in fact are not connected with Metazoan evolu�tion. The distribution of vendobionts in the aphoticzone of the ocean or their existence under the surfaceof the sediment excludes their possible algal sensu latoaffinity and the presence of photosymbionts (Grazh�dankin, Seilacher, 2002; Peterson et al., 2003). Like�wise, they are not directly related to fungi or lichens,with which they are sometimes compared (Retallack,1994; Peterson et al., 2003), because the continuousfractal�like system of canals of various cross�sections,as well as the tube�like chambers characteristic of ven�dobionts, had nothing in common with the cylindricalhyphae of fungi, which at comparable length are sub�

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Fig. 4. Cambrian (a–u) and Ordovician (e) Lophotrochozoa: (a, b) – “tommotiids” (a) Paterimitra, (b) Camenella (c, d) celo�sclerites�loclescleritophores: (c) Halkieria, (d) Allonnia (Chancelloriida), (c) annelid Plumulites (Machaeridia). Animal recon�structions with measurements are given according to Bengtson (1970); Conway Morris and Peel (1995); Bengtson and Hou(2001); Vinther et al. (2007); Larsson et al. (2014). © Artist Vsevolod Abramov.

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divided by septa. This branching system of canals/chambers allowed vendobionts to absorb dissolvedorganic matter forming compact multitiered bottomcommunities (the upper tier reaches 2 m) in environ�ments with very slow currents (not more than 1–5 cm/s)(Burzin et al., 1998; Sperling et al., 2007; Lafammeet al., 2013; Ghisalbert et al., 2014) (Figs. 3b and 3d).This system of canals, chambers and frondlets, whichenable the organism’s growth, allowed vendobionts toretain a body area to volume proportion of 1 × 1000 ×102 mm–1, whereas this ratio in osmotic mega�bacteriareaches 1 × 101 mm–1 or more, although their size doesnot exceed 0.75 mm (Lafamme et al., 2009). Biome�chanical experiments with plastic models of lobe�likestalked vendobionts in tanks showed that the “quilted”relief directed the water current along the body sur�face, whereas the resulting vibration of the lobe, bend�ing parallel to the current, reduced the load of the cur�rent and at the same time boosted the exchange of flu�ids with the environment by facilitating the diffusionof dissolved matter. The current rate dropped due tothe relief of the lobe, while the mixing of the watermass along the lobe increased (Singer et al., 2013).Suspension feeding required a constant, relativelystrong (over 5 cm/s) current, three�dimensional filter�ing organs (flagellate chambers of sponges, lopho�phore of brachiopods, gills and bivalve siphons),whereas the suspension feeder should be positionedperpendicular to the current (Vogel, 1988) and notbent along it (like thalli of ribbon�like algae), as is sug�gested for vendobionts.

Vendobionts lying freely on the bottom and thoseliving in the subsurface growing through the substrateor even through adjacent (already dead?) individualswere also osmotrophs (Grazhdankin and Seailacher,2002; Droser et al., 2014), because they are organizedexactly like stalked taxa (Figs. 3a, 3c, and 3e–3i).Traces of vendobionts are traces of absorption, engulf�ing, and the showing of imprints of the branchingcanal system (Ivantsov, 2011, pl. 2, fig. 4). They couldonly appear if the organism was very tightly sucking onthe substrate by its entire surface. An unusual, discretemovement of vendobionts to a distance not greaterthan a third of their length (Ivantsov and Mala�khovskaya, 2002; Ivantsov, 2011), as well as a slightreduction of the surface (Brasier and Antcliffe, 2008),were apparently performed by the same systems ofcanals. A change in osmotic pressure would allow thesurface area to be decreased and remove the organismfrom the substrate. For further movement at the sur�face to volume ratio, even a small current or low waveswould be sufficient. A similar mechanism is presentlyused by predatory fungi, which are able (in 0.1 s) toabsorb more water into the cells and increase their vol�ume, catching and immobilizing a round worm or awater bear, by changing the osmotic pressure in thehyphae quickly (Heintz and Pramer, 1972; Chen et al.,2001). The fungal activity is initiated by a change inthe concentration of different elements (e.g., C/N) in

the environment. In the event of an exhaustedresource, e.g. precipitated organic suspension or bac�terial mat, such a signal would be also detected by avendobiont.

The content of dissolved, colloidal, and suspendedorganic matter in the Ediacaran ocean was 2–3 timeshigher than the present level, which is determined bythe proportion of the isotopes of Ca, N and organiccarbon (Fike et al., 2004; Shields�Zhou and Zhu,2013; Kikumoto et al., 2014). It is no coincidence thatother giant osmotrophs are characteristic of the Edi�acaran: bacterial colonies and fungi (Marusin et al.,2011). In the modern oceans, megabacteria, the largestosmotrophs, are concentrated in upwelling zones, i.e.,in conditions of a stable biogene flux (Schulz, H.N. andSchulz, H.D., 2005). The diversification of vendo�bionts began in the zone of counter currents andupwelling of the subpolar sea (Fedonkin, 2000;Lafamme et al., 2013) and continued in an environ�ment of increased content of oceanic organic matterwith frequent drops in the oxygen level and theabsence of bioturbators and predators. A decrease inthe significance of the first of these factors and a sharpincrease in the significance of the latter led to a com�plete disappearance of vendobionts at the Ediacaran–Cambrian boundary. The carbon isotope anomaliesrecorded for the deposits of this age suggest a largeturnover of the carbon cycle, which has no equivalentin the Earth’s subsequent history. Although the occur�rence of vendobionts from younger deposits are fre�quently mentioned (e.g., Conway Morris, 1993; Bab�cock and Ciampaglio, 2007), none of these recordsmeet the above morphological criteria. They eitherrepresent the remains of normal Phanerozoic organ�isms, or fossil traces, or sometimes inorganic struc�tures.

The morphology of Ediacaran skeletal organisms isinteresting. For instance, the most common of them,Cloudina, has a very unusual skeleton consisting ofeccentric calcareous cones nested within one anotherand with closed bases; the microstructure of the skele�ton is primitive and is found in red and other calcare�ous algae (Viridiplantae), foraminifers (Rhizaria),sponges and Cnidaria (lower Metazoa); in annelids,including pogonophores, this microstructure is notfound. No protoconch has been found in Cloudina,but a basal opening is present (Cortijo et al., 2010;Vinn and Zaton, 2012; Zhuravlev et al., 2012). Nama�calathus has a calcareous skeleton in the shape of aporous polyhedron on a stalk. No stolon or polypoidcharacters are observed (Grotzinger et al., 2000).Namapoikia is a shapeless honeycomb mass. Suvorov�ella and Majaella are possible skeletal vendobionts,Sinotubulites is a cylindrical shell of irregular layers ofaragonite. Anabarites is spirally coiled conical shellswith three lobes (Vologdin and Maslov, 1960; Kouchin�sky and Bengtson, 2002; Wood et al., 2002; Chenet al., 2008; Zhuravlev et al., 2012). All of these earli�est skeletal organisms disappeared at the end of the



Ediacaran–beginning of the Cambrian period and, inlight their unusual morphology, have nothing in com�mon even with the subsequent Cambrian “explosion.”Namacalathus (see below).

Sponges: Not Spicules Only

Sponges are widely believed to be the first Metazoain the fossil record, although all early occurrences ofthese organisms are debatable. Biomarkers (indestruc�tible remains of some aromatic and aliphatic hydro�carbons (Peters and Moldowan, 1993; Summonset al., 2006)), i.e., 24�isopropylcholestanes, specificfor this group and abundant in the Ediacaran oil�bear�ing and carbonate deposits, suggest that sponges couldhave existed 635 Ma (Love et al., 2009). However,Love et al. do not exclude the possibility that these aremolecular remains “of their ancestors” (Love et al.,2009, p. 719). It is quite possible that these biomarkersbelong to algae (Stramenopiles) and are diageneticallyaltered (Antcliffe, 2013). Reitner and Wörheide(2002) recorded spicules in the cryogenic dolomiteNoonday (750 Ma) in Nevada; illustrations of the spi�cules have not been published, but this paper is oftencited as a primary source (Müller et al., 2007; Sperlinget al., 2010). The same authors published a photo�graph of a “speculate sponge” from the Vendian of theWhite Sea Region, which is possibly a stalked vendo�biont similar to Palaeophragmodictya spinosadescribed in the same locality by Serezhnikova (2007).The tube itself, which is a Palaeophragmodictya speci�men from Ediacara Hills (Gehling and Rigby, 1996),has a fractal structure of canals typical of Osmotro�pha–vendobionts rather than sponges that are suspen�sion feeders. Late Ediacaran spicules from the TsaganOlom Formation of Mongolia (Brasier et al., 1997)were shown to be inorganic mineral crystals (Antcliffeet al., 2011). It is difficult to imagine that the Ediaca�ran Coronacollina (Clites et al., 2012) was a sponge. Ithas a prefect tetraradial arrangement of spicules of thesame number in differently sized specimens of this fos�sil (from 1 to 22 mm across), which more likely sug�gests a mineralogical origin. New sponge�like organ�isms continue to be reported from ancient beds: e.g.,unusual, possibly skeletal remains from the TrezonaFormation (660–635 Ma) in South Australia (Maloofet al., 2010b) and Otavia in rocks from 760–635 Ma inNamibia (Brain et al., 2012), but the assignment ofthese fossils to sponges, or to the Metazoa in general,remains unsubstantiated.

The sponge record begins in the Cambrian Periodwith the appearance of Hexactinellida, Demospon�giae, and Calcarea known from spicules of a certainsymmetry type and chemical composition, as well ascomplete skeletons (Fig. 1). Only Homoscleromorphaare not confirmed in the fossil record. In contrast,there were several extinct groups of sponges in theCambrian Period: heteractinids and archeocyaths.The latter were the most prolific and became largely

extinct within the Early Cambrian, with only two spe�cies known from the Middle and Late Cambrian beds.Since both were suspension feeders, the assignment ofarchaeocyaths to sponges is supported by biomechan�ical studies of skeleton models, usually a porous cupwith vertical and/or horizontal porous septa connect�ing walls in tanks (Savarese, 1992), and the analysis oftrends in evolutionary changes in their skeletal ele�ments toward improving filtration (Zhuravlev, 1993b).Judging from the skeletal microstructure, body plan,and the nature of asexual reproduction and immunereactions (fossil reefs retain skeletons in lifelike posi�tions and in relationships with related and unrelatedorganisms), archaeocyaths were most similar to mod�ern sponges, which include taxa with calcareous skel�etons with no spicules, similar to the skeleton ofarchaeocyaths, Acanthochaetetes, and Vaceletia(Zhuravlev, 1989; Debrenne and Zhuravlev, 1994)(Fig. 1). Hemispherical radiocyaths were the largestabundant, though not diverse, Cambrian reef buildersof supposedly sponge affinity. Their skeleton was com�posed of dumbbell�like elements with stellate plates onthe ends, which, by contact with rays, formed porousouter and inner walls. Their only equivalents andprobable descendants were Ordovician–Permianreceptaculids, in which the stellate plates were overtime replaced by solid rhomboid plates (Zhuravlev,1986).

Botting and Butterfeld (2005) collected interestingmaterial on heteractinids (fossil sponges) with skele�tons composed of regular multiradiate spicules (whichwas the reason behind their assignment to a separateorder within the Calcarea). The authors found in theearliest heteractinid Eiffelia bilayered hexaradiate andtetraradiate spicules of several orders, in which thecore is composed of high�magnesium calcite and theexternal layer is composed of silica (opal) (Fig. 1).Since the hexaradiate siliceous spicules are found onlyin hexaactinellids and calcite tertraradiate spicules aretypical of the calcareous sponges, it was suggested thatheteractinids were transitional taxa from Silicea toCalcarea. This hypothesis was supported by phyloge�netic analysis of microRNA (Sperling et al., 2010) andalso by the appearance of spicules in calcareoussponges later in the fossil records than spicules ofhexaradiate and common sponges (Zhuravlev andWood, 2008).

Cnidaria: Where the Jellyfish Swam?

Most Ediacaran organisms have previously beenconsidered members of Cnidaria, mainly jellyfish andsea pens (Octocorallia) (Glaessner, 1984; Jenkins,1992). However these “sea pens” are vendobionts,whereas Ediacaran “jellyfish” represent vendobiontattachment discs or colonies of algae and/or bacteria(Grazhdankin and Gerdes, 2007; Serezhnikova, 2007,2013). Cambrian “jellyfish” were more diverse; someof them were fossil traces (Jensen et al., 2002); brachi�

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opods (Zhang et al., 2009); Xenusia (Ramsköld andChen, 1998); paropsonemids; pelagic organisms witha multilobed, possibly chitinized, swimming disc, andsuspended spirally coiled gut with a crown of branch�ing tentacles around the mouth; animals comparedwith lophophorates and deuterostomes (Friend et al.,2002; Zhu et al., 2002); and even the mouthparts ofextinct Ecdysozoa (Anomalocarididae) (Whittingtonand Briggs, 1985). Possible jellyfish imprints areknown only from the Middle Cambrian (Young andHagadorn, 2010). Their affinity to any extant groups isnot established, although statements to the contrarycan be found in the literature. For instance, Cart�wright et al., 2007, based on 120 specimens, describedjellyfish representing three modern classes and four fam�ilies (Hydrozoa, Scyphozoa (2), and Cubozoa). How�ever, all four have the same “umbrella” size (7–8 mm)and number of “tentacles” (about 18), whereas theauthors determined the presence of any diagnosticcharacters from imprints of various preservation statesor the position on the bedding surface. In other words,this is either a species combining characteristics of allthree modern classes or not a jellyfish at all.

The earliest Cnidaria, with mineral and chinitizedskeletons, appear only in the Cambrian Period, i.e., atleast 30 Ma earlier than the aforementioned MiddleCambrian “jellyfish”. They were at first very simplesingular organisms; after 10–15 Ma, they were modu�lar forms similar to Ordovician corals (Tabulata)(Zhuravlev et al., 1993; Zhuravlev, 1999; Fuller andJenkins, 2007; Park et al., 2011) (Fig. 1). Apart fromthese, the possible Cnidaria included Hexaconularia(sessile organisms with phosphatic (or post�mortemphosphatized) skeletons in the shape of an upturnedhexagonal pyramid), which are only known from thebasal Cambrian of South China and India, and conu�lariids with a fourfold organic, or probably chitinized,skeleton covered on the top. Conulariids appeared inthe Late Cambrian, and hexaconoluriids are com�pared to Stauromedusae, if tetraradiate symmetry isconsidered as a major character, or with Coronata, ifstrobili�like constrictions are taken into account(van Iten et al., 2006, 2010). Hexaconularia includesome Cambrian embryos known as Punctatus andOlivoodes and resemble juvenile coral polyps includedin the peridermis (Bengtson and Yue, 1997; Dong etal., 2013). However, some Olivoodes and “soft corals”have a pentaradial symmetry instead of tetraradial, aswell as micrornamentation, which does not excludetheir possible affinity to Ecdysozoa (Liu et al., 2014;Steiner et al., 2014). The same group of jellyfish pre�sumably includes the hyolithelminthes Byronia andSphenothallus, represented by phosphate tubes withtransverse ribbing and microlamellar microstructurecommon in the Cambrian rocks (Bischoff, 1989;van Iten et al., 1992; Zhu et al., 2000; Vinn, 2006).These are often compared with annelids or pogono�phores, but their microstructure and the presence of

attachment discs and pseudocolonies in the two lattertaxa suggests their cnidarian affinity.

The history of Cnidaria, like the history ofSponges, contradicts Dewel’s (2000) hypothesis thatBilateria could have evolved from clonal animals likesea pens, the colonial organization of which gave riseto the triblastic ancestors of Bilateria. Dewel consid�ered sea pens to be Vendobiota, a fossil group that hadno connection to the origin of Bilateria and Metazoa.If the fossil record is taken into account, the first fossilorganisms in each major branch of Bilateria—Ecdys�ozoa, Lophotrochozoa and Deuterostomia—repre�sent the remains of of nonclonal organisms capable ofmovement. Moreover, even among confirmed fossilsponges and cnidarians, all of the earliest representa�tives are solitary organisms. For instance, a represen�tative statistical sample (all 305 known genera) of theearliest archaeocyaths were solitary organisms, andthey only later gave rise to the first branching (modu�lar) and, later, massive (multimodular) taxa (Wood etal., 1992). The term “modular” is used here becauseall colonial organisms are modular, i.e., they consist ofmodules, but not all modular organisms can be con�sidered colonial. For instance, in most archaeocyaths,the modules are separated by secondary skeletaldeposits that in the live animal gradually lost their con�nection to one another, even if they developed bybranching or budding from the same paternal individ�ual. The same applies to the Cambrian speculatesponges (Hexactinellida, Demospongiae, Calcarea).The solitary forms are the first to appear in the fossilrecord, and only much later do very rare modular taxaappear. Their complete skeletons, not disassociatedinto separate spicules, are found in Lagerstätten andlithified reefs (Rigby and Hou, 1995; Rigby and Col�lins, 2004; Ivantsov et al., 2005; Kruse and Zhuravlev,2008; Wu et al., 2014). In general, of the 4367 generaof Cambrian fossil organisms known by 2001, only3.5% are modular taxa (archaeocyaths, radiocyaths,and other sponges—75 genera; coralomorphs—25;bryozoans—2; graptolites and pterobranchs—48)(Wood et al., 1992; Zhuravlev, 2001). In the lastdecade, another 400 genera were described, of whichno more than 5 are modular, so their total proportiondecreased. None of these taxa is an early ancestor ofany group of Metazoa.

Deuterostomes (With and without Inverted Commas)

Although a third of Cambrian modular organismswere hemichordates, the earliest Deuterostomia werenot colonial organisms. Among hemichordates, pter�obranchiates appeared only inthe Middle Cambrian,and the earliest of these are very simple solitary taxa—“Rhabdopleura” and Cephalodiscus(?) (Durman andSennikov, 1993; Harvey et al., 2012). Their aggrega�tion presumably resulted in the appearance of simplecolonial organisms (Maletz, 2014). A further increase



in the complexity of blastogenesis occurred in grapto�lites (Cooper et al., 1998). The pterobranch affinity ofall these taxa was established based on the morphologyof the tubular organic skeleton, which in pterobranchs(coenecium) and graptolites (rhabdosome) is com�posed of collagen fusellar layers (Mierzejewski andKulicki, 2001).

The problematic earliest Cambrian pterobranchs,Galeaplumosus and Herpetogaster, represent imprintsof solitary organisms with crowns of feathery tentaclesand without a coenecium (Caron et al., 2010; Houet al., 2011). Their pterobranch affinity is not con�firmed, because the zooids of pterobranchs degradewithin a few days, losing all distinct characters of aclass or even a phylum (Briggs et al., 1995). In additionthe tentacles of modern pterobranchs develop from amesosoma, or collar, rather than from the prosoma, orhead shield (anterior region), where they occur(Maletz, 2014).

The two Middle Cambrian fossils, which were pre�viously assigned to annelids or priapulids, Oesia andSpartobranchus are more interesting. Their large (upto 10 cm) wormlike body with a straight gut is subdi�vided into three regions. The second possesses numer�ous gill slits, whereas the mouth opening in Sparto�branchus occurs at the border of the head and neckregions, and the head region contains structuresresembling a stomochord and “Y�shaped structure”(Conway Morris, 2009; Caron et al., 2013a) (Fig. 1).However, it has an external organic tube embracingabout a quarter of the organism’s length, which some�times branches. This tube could be ancestral to thecoenecium of pterobranchs. The sister�group rela�tionships of Pterobranchia and Enteropneusta aresuggested by molecular and comparative anatomicalevidence (Brown et al., 2008; Swalla and Smith, 2008;Philippe et al., 2011), which does not exclude the pos�sibility of the Pterobranchia having evolved fromEnteropneusta.

As for the occurrences of the Early Cambrian chor�dates, the presence in the presumed tunicates (Che�ungkongella, Phlogites, Shankîuclava; Shu et al., 2001;Chen et al., 2003) of tentacle�like structures is mostsimilar to the body plans of tentaculate animals(Caron et al., 2010; Shu et al., 2010). It is quite possi�ble that the “soft�bodied pterobranchs” and “tuni�cates” are the remains of tentaculate animals pre�served due to chitinization of their external covers: the“tunicates” strongly resemble Cambrian brachiopodswith a nonmineralized shell (they have structures likea pedicle, shells, and the lophophore), whereas Herpe�togaster is distinguished from the paropsonemids dis�cussed in the previous section only in the absence of aswimming disc. Interestingly, Cheungkongella has pre�viously been considered a hypothetical pentaradiateancestor of chordates, although its poor state of pres�ervation and the absence of the side presumably withthe mouth opening, do not allow any considerations ofits symmetry.

Problematic genera assigned to chordates (Pikaia,Metaspriggina, Yunnanozoon, Cathaymyrus, Haik�ouella, Myllokunmingia, Haikouichthys, andZhongjianichthys) appear in the Lower and MiddleCambrian–Chengjiang and Burgess Shales, respec�tively (Chen et al., 1995a, 1999; Shu et al., 1996, 1999,2003a; Shu, 2003; Conway Morris, 2008; ConwayMorris and Caron, 2012). Yunnanozoon and Haik�ouella, as well as Myllokunmingia and Haikouichthys,apparently represent different forms of preservation ofthe same taxa; and the differences between them arenot greater than of species level (Hou et al., 2002;Chen and Huang, 2008). The Middle CambrianPikaia, which was the first of the fossils to be inter�preted as a chordate, has antenna�like appendages inthe head region and almost flat borders of the myo�tomes, which suggests the absence in this taxon of asystem of muscles typical of chordates (Lacalli, 2012).In contrast, Yunnanozoon, despite the presence of asegmented dorsal crest, strongly agrees with the bodyplan of this phylum: the crest, which resembles a V�shaped myosepta, could be an additional support formuscle blocks, reducing the load on the myosepta andthereby facilitating active swimming movements(Lacalli, 2012) (Fig. 1). Although Cambrian fossils,which are described as chordates, are difficult to inter�pret, the number of Yunnanozoon specimens reachesmany hundreds, and therefore, despite taphonomicdistortion (making it impossible to establish the pres�ence of a notochord), it is possible to assume reliablythe presence in this group of V�shaped myotomes, gillslits connected with the gut, gill arches, paired gonads,and a postnatal caudal region, which indicates a chor�date affinity (Shu et al., 2003b, 2010; Donoghue andPurnell, 2009; Lacalli, 2012). This is supported byexperiments on postmortem changes in the remains ofmodern Cyclostomata and other chordates (Sansom etal., 2011). Although the features of Yunnanozoon, aswell as Cathaymyrus and Metaspriggina known fromindividual specimens, agree with the body plan ofcephalochordates, Myllokunmingia, with its dorsaland ventral fins and nasal capsules, can be consideredthe earliest chordate (Hou et al., 2002; Conway Mor�ris, 2008; Shu et al., 2010). The remains of the littleknown Zhongjianichthys (Shu, 2003) are unfortunatelytoo incomplete to make any hypotheses of its affinity.

Odontogriphus from the Burgess Shale, despiterecent attempts to assign it to the soft�bodied mol�lusks, possibly belongs to the Cambrian Deuterosto�mia (Caron et al., 2006; Conway Morris and Caron,2007; Smith M.R., 2012). It needs to be noted that, ofall Molluscan features, this taxon has only a mouthopening surrounded by teeth, which are compared toa radula, whereas its body, with a pronounced trans�verse segmentation, does not correspond to this plan(Conway Morris, 1976; Butterfeld, 2006). This mor�phology of Odontogriphus could equally suggest anaffinity to chordates; as with Yunnanozoon, this is sup�ported by a type of preservation not typical for mol�

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lusks. This similarity was recently emphasized bySmith (2012), who studied 165 specimens of mouthapparatus of Odontogriphus and made significant argu�ments as to why this fossil cannot be an annelid: themultirowed mouth apparatus, the presence of a basalmembrane, and the probability of supporting appara�tuses. One important observation listed by Smith (butnot discussed, as he considered Odontogriphus to be amollusk) shows that this animal could not be a mol�lusk: the tooth cavities contain increased concentra�tions of Ca and F, which are absent elsewhere in thebody. This means that the teeth in Odontogriphus werecalcium�phosphate, like the teeth of chordates.

The latter include the multiple phosphate teeth ofconodontophorides, which (conodonts) were wide�spread from the Middle Cambrian up to the TriassicPeriod. Only three Paleozoic localities containimprints of the conodontophoride body. The imprintsreveal large eyes, complex tooth apparatus, gill slits, V�shaped myotomes, and a tail with a caudal fin (Ald�ridge and Briggs, 1986; Donoghue et al., 2000) (Fig. 1).However, the teeth are most important to understandthe affinity of these animals. The teeth have three lay�ers, including enamel and dentine, suggesting thatthey belonged to jawless vertebrates, most likely activepredators (Barskov et al., 1978; Donoghue, 2001;Goudemand et al., 2011; Nemliher and Kallaste,2012).

It is thought that the notochord in Yunnanozoon,Cathaymyrus, and Myllokunmingia occurs on the dor�sal side, above the gut (Chen et al., 1999; Shu et al.,1999). However, it is difficult to determine positivelywhich fossil structures correspond to this organ. TheYunnanozoon has a rod�like structure under the gutwhich is not thought to be a notochord, because “thepurported yunnanozoan notochord is in a ventralposition where it could not act as an antagonist” (Shuand Conway Morris, 2003, p. 1372d). However, tointeract with the muscles, Yunnanozoon had a seg�mented crest, whereas the notochord could also havefunctioned in the same way, if it was in the dorsal posi�tion. Indeed, this organ could not have shifted byitself, whereas the cephalochordates could have had it,as was shown by Malakhov (1977), judging from thebehavioural features of Amphioxus (cephalochordate)and the fact that the body plan of Enteropneustaexactly mirrors that of Chordata (position of the pro�tocoel, coelomic openings, neural plate, blood flowdirection, and incipient blastopore). Geoffroy Saint�Hilaire (1822) tried to prove the same hypothesis, but190 years ago he could not refer to the evidence pro�vided by molecular biology. Data on the expression ofregulatory genes in the ontogeny of the nervous systemand “general marker genes ” during gastrulation (invertebrates Chd marks the dorsal side and BMP�4/2marks the ventral side, and their orthologs in insects,Sog and Dpp, vice versa mark the ventral and the dor�sal sides) confirmed that the dorsal neural cord of ver�tebrates is homologous to the ventral neural chain in

annelids and arthropods (Arendt and Nubler�Jung,1994; Brown et al., 2008; Lowe, 2008; Nomaksteinskyet al., 2009). The new (“dorsal”) mouth opening inmodern Amphioxus opens in place of a gill slit (Benito�Gutierrez and Arendt, 2009), but the mouth wasalmost terminal rather than ventral in the CambrianYunnanozoon (equivalent of Amphioxus).

In a sense, the subdivision of Bilateria into pro�tostomes and deuterostomes lost its usefulness,because, even in Priapulida, the blastopore gives rise tothe anus at the vegetal pole, following strictly a deu�terostomic pattern. Moreover, the succession ofexpression of regulatory genes during the formation ofthe blastopore, mouth, and anal opening is the same inpriapulids and deuterostomes (Martín�Durán et al.,2012).

In total, the paleontological and molecular data, aswell as embryological studies, suggest that tunicateswere not a group that evolutionarily preceded cepha�lochordates or even vertebrates. It is possible that theyare secondarily simplified; they lost some of theirHox�genes and, along with them, nephridia and tracesof metamere structure (Delsuc et al., 2006; Brown etal., 2008; Putnam et al., 2008; Cannon et al., 2009;García�Fernàndez, Benito�Gutiérrez, 2009; Smith A.,2012; Caron et al., 2013a; Maletz, 2014). Whateverplace the Cambrian chordates might have occupiedamong deuterostomia, primitive cephalochordates, orvertebrates, they were solitary (nonclonal) motile nek�tonic or nektobenthic organisms. Moreover, the pres�ence of the phosphate inner skeleton in vertebratesindicates that their ancestors were motile and veryactive animals, because high muscle activity results ina decrease in pH in the inner medium of the organismup to the level at which only the phosphatic skeletonremains insoluble (Ruben and Bennett, 1987; Woodand Zhuravlev, 2012). If the first chordates were poorswimmers like Amphioxus, their skeleton would haveto be built of energetically more efficient carbonate,like echinoderms.

Cambrian echinoderms can easily be recognized,even from separate plates with a stereomic structurethat is found only in this phylum and always consists ofhigh�magnesium calcite. Four main groups are recog�nized among these echinoderms based on the bodyplan and the presence of ambulacra: (1) bilaterallysymmetrical, without ambulacra (Ctenocystoidea);(2) asymmetrical, both with and without ambulacra(Cincta, Soluta, and Stylophora, also known as Car�pozoa); (3) spirally symmetrical, with numerousambulacra radiating from the mouth opening (Helico�placoidea); and (4) pentaradial with a pentaradialarrangement of ambulacra (Edrioasteroidea, Rhomb�ifera and Eocrinoidea sensu lato) (Zamora and Smith,2012; Smith et al., 2013). Early Cambrian echino�derms include taxa with perfect bilateral symmetry(Ctenoimbricata, Courtessolea) that are morphologi�cally intermediate between the classes Ctenocystoideaand Cincta, which some authors consider basal for all



echinoderms; the periproct and the anal pyramid inthese taxa occur on the posterior end of the body, indi�cating a straight rather than U�shaped gut (Zamoraet al., 2012) (Fig. 1). Occurrences in the Middle Cam�brian of Spain and France of juvenile Cambraster fromthe class Edrioasteroidea show that these perfectlypentaradial attached echinoderms in early ontogenyretained bilateral symmetry (Zamora et al., 2013, fig. 7).Edrioasteroidea are considered a likely stem group forall Eleutherozoan echinoderms (starfish, sea urchins,sea cucumbers, and brittle stars) (Rozhnov, 2012).These paleontological data are supported by molecu�lar biology: echinoderms retain the ancestral complexof genes characteristic of a bilaterallysymmetricalbody plan similar to that in an ancestor shared by alldeuterostomes, whereas the similar larva—dipleurula,along with molecular data, allows their considerationas a sister group of hemichordates within the Ambu�lacraria (Morris, 2007).

Pentaradiality (or simply radiality), a key characterof the echinoderm phylum, is absent in many earlyechinoderm taxa. These can be recognized from thestereome structure of skeletal elements resulting fromhighly cooriented mineral nanoparticles formed fromamorphous precursors of high�magnesium calcite.They give the optical qualities of a single crystal to theentire porous element (Killian et al., 2009). Since theskeletons of chordates and echinoderms were funda�mentally different from the very beginning of thesegroups, the old and now forgotten calcichordate cla�distic hypothesis, according to which chordatesevolved from asymmetric Cambrian echinoderms(Carpozoa) (Jefferies, 1986), was shown to be unsub�stantiated. Cladistics helps very little to interpret pale�ontological material, because in this case it is impossi�ble to analyze hundreds and thousands of homologousequally weighted characters (as in molecular biologyor in structural linguistics). Therefore, the composi�tion of the stem and terminal groups significantlychanges in each new cladogram (see Wills, 1995; Legget al., 2012, 2013). Nevertheless, a series of terms usedin cladistics, for example “synapomorphy,” “stem,”and terminal groups, turn out to be more useful than“ancestors” and “descendants” to characterize fossilsof a higher rank that do not fit the framework of phylaand classes outlined in the modern material, e.g. Cam�brian echinoderms.

Along with echinoderms, hemichordates, andchordates, the Cambrian Lagerstätten often containthe remains of one or two other groups, Vetulicolia andBanffozoa (named after the typical genera Vetulicolaand Banffa), which are lately assigned to Deuterosto�mia and, more precisely, to chordates. These organ�isms, which are a few centimeters in length, aredescribed as a bilaterally symmetrical and clearly sep�arated into an anterior section covered by a carapace,with gill slits opening into the gut, and with filaments,endostyle, and a dorsal fin, whereas the posterior endhas the appearance of a segmented tail (Gee, 2001;

Aldridge et al., 2007; Shu et al., 2010; Vinther et al.,2011; Ou et al., 2012a). These remains can be inter�preted differently: a carapace with cellular ornamen�tation and a segmented tail (Briggs et al., 2005; Caron,2006; Bergstrom, 2010; Zhuravlev et al., 2011b) (Fig. 2j).In the former case, the resulting organism had thecharacteristics of a chordate and hemichordate butwith a segmented tail. In the latter case, it had thecharacteristics of a legless arthropod. The latter havecellular carapaces and a thin folded structure (Butter�feld, 2002). Even when this description is supple�mented by another important characteristic, i.e., a ter�minal mouth opening with cyclically arranged toothplates, this will not clarify the problematic affinity,although the hypothesis of the deuterostome affinity ofVetulicolia and Banffozoa seems to be not very consis�tent. These animals cannot be assigned to arthropods,since they lack a key feature. Perhaps these were earlymembers of Ecdysozoa, which could include onlypartly segmented animals like anomalocaridids, whichare different from Vetulicolia only in the presence ofmouthparts and compound eyes.

Ecdysozoa: Abundant Fruit of Arthropodization

The concept of arthropodization, which was ele�gantly used by Ponomarenko (1998, 2004), aptlyexplains the main evolutionary processes of the Cam�brian Period: segmented appendages (arthropodiza�tion s.s.) and carapaces (arthrodization) indepen�dently appear not only in arthropods (probably morethan once) but also in anomalocaridids, some xenu�sians, and vetulicolians. These animals, along withtheir wormlike relatives, essentially cleared Canfield’socean due to bioturbation, the establishment of a fecalpellet conveyor belt, and the creation of a multitieredtrophic pyramid with predators of several orders. Theyeventually made it suitable for life in all its diversity.Unsurprisingly, the remains of Ecdysozoa, as men�tioned above, constitute 70% of Cambrian fossils intheir diversity, number of individuals, and biovolume,thereby comprehensively representing their evolution.

Although many zoologists still think that the con�cept of the generalized “body plan,” hard won by cen�turies of comparative anatomy studies, is underminedby phylogenies based on molecular data, this is farfrom true. The “centuries�old tradition” was discon�tinued with the development of completely new tech�nology of molecular studies but also by technologyallowing insight into the smallest living organisms atany stage of their evolution and their fossil remains.Therefore, a revision of previous concepts about therelationships between the phyla and classes alsooccurred in modern morphological, embryological,and paleontological research. Interestingly, the idea toconnect nematodes and arthropods (insects) is notnew, and, despite common belief, it was not put for�ward by molecular biologists. It was Odo Reuter (aFinnish entomologist) who was the first to note the

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similarities in the chitinous covers, absence of cilia,reduced ability to regenerate, and the absence of thering muscle in these groups (Reuter, 1913; Lyubish�chev, 1982). Reuter can be considered the pioneer ofthe ecdysozoan hypothesis.

The Ecdysozoa has three important characters(synapomorphies): embryonic development, structureof the cuticle, and, to some extent, the morphology ofthe mouth apparatus. It is worth noting the his�tochemical similarity of the nervous system of Ecdys�ozoa (arthropods, onychophorans, priapulids, nem�atomorphans, and nematodes), revealed in the similarexpression of components during immunohistochem�ical staining by certain ferments, which do not causesimilar reactions in cnidarians, ctenophores, annelids,mollusks, rotifers, chaetognaths, bryozoans, or deu�terostomes (Haase et al., 2001).

Ungerer and Scholtz (2009, p. 272) considered thatnew studies of the embryonic development of pyc�nogonids, as well as arthropods (Alwes and Scholtz,2004), tardigrades (Hejnol and Schnabel, 2005), nem�atodes (Schulze and Schierenberg, 2008), priapulids(Wennberg et al., 2008), and kinorhynchs (Kozloff,2007), reveal “… holoblastic, irregular radial, regularto nearly regular cleavage and a gastrulation specifiedby large division�retarded immigrating blastomere fol�lowed by smaller immigrating blastomeres.” This typeof embryogenesis was likely to be initial for all Ecdys�ozoa lacking spiral cleavage, ciliated larva, or a larvawith an apical plate or apical tuft.

The cuticle of Ecdysozoa is composed of laminateepicuticle secreted by the microvilli of epidermal cellsand the protein exocuticle and endocuticle composedof α�chitinous fibers, which are assembled in spiralplates. A complete change of the cuticle (molting)occurs at least once in the lifetime; it is induced by ste�roid hormones (ecdysones), as was demonstrated foronychophorans, tardigrades, arthropods, priapulids,kinorhynchs, loriciferans, and nematophorans (Robson,1964; Crowe et al., 1970; Plotnick, 1990, Schmidt�Rhaesa et al., 1998; Lemburg, 1999; Nielsen, 2001;Schmidt�Rhaesa, 2006; Al�Sawalmih et al., 2008).The formation of the cuticle, like molting in Ecdyso�zoa, is controlled by the same group of regulatorygenes of the hormone�receptor NHR�23 complex(Kouns et al., 2011). Although the cuticle lacks chitinin adult nematophorans, α�chitin fibers are present inthe basal layer of the larval cuticle, as in the lorica ofthe priapulid and loriciferan larvae (Neuhaus et al.,1996); in nematodes, the α�chitin cuticle is preservedin the pharyngeal region (Neuhaus et al., 1997). Inannelids, the cuticle is totally different: its layers areformed by collagenous cords composed in a quasior�thogonal lattice penetrated by numerous protuber�ances of epithelial cells; it lacks chitin. β�chitin ispresent only in setae; mollusks, brachiopods, and bry�ozoans have γ�chitin (Plotnick, 1990). The thickmolting cuticle of Ecdysozoa precludes the develop�ment of any kind of ciliated epithelium, even in larvae.

Such an epithelium develops in Lophotrochozoa, andthe cuticle in this group is never molted entirely but isreplaced in patches (Schmidt�Rhaesa et al., 1998). Anecdysozoan�like cuticle is present in at least two Cam�brian groups: Palaeoscolecida (primitive cephalo�rhynchs) and xenusians (onychophoran�like organ�isms with terminal position of the mouth opening)with phosphatized culticular layers. Collagen fibers areof course absent in fossils, but numerous cavities thathoused them are distinctly visible (Zhuravlev et al.,2011b). Larval sheaths are known in various fossilcephalorhynchs, xenusians, and arthropods, some ofwhich were buried during molting (Müller and Hinz�Schallreuter, 1993; Garía�Bellido and Collins, 2004;Topper et al., 2013b).

The radial symmetrical retractile proboscis (intro�vert) is a very important organ, which, apart from thenervous center, includes a system of retractory musclesand has numerous concentric rows of hollow sensory�locomotory spines (scalids). The introvert, which isused for orientation, searching, and grasping food,and locomotion, is present, at least at the larval stage,in the Priapulida, the Loricifera, the Kinorhyncha,and the Nematomorpha (which Malakhov (1980;Malakhov and Adrianov, 1995) included in the phylumCephalorhyncha and Nielsen included (1995) in theIntroverta (including the Nematoda) (Eriksson andBudd, 2001; Liu et al., 2014)). Some pycnogonids alsopossess an introvert (Nielsen, 1995), while pyc�nogonids have a nonretractable proboscis and a trira�diate pharynx typical of some cephalorhynchs andnematodes (Eriksson and Budd, 2001b; Liu et al.,2014). There are also fossil Jurassic pycnogonids witha hypertrophied proboscis (Charbonnier et al., 2007).Tardigrades have a prominent telescoping mouth conesurrounded by a ring of plate�like peribuccal lamellaethat resembles a kinorhynch mouth cone and a tri�radial bucco�pharyngeal apparatus armed with teeth(Dewel, R.A. and Dewel, W.S., 1997; Kristensen,2002; Dewel and Eibye�Jacobsen, 2006). A nonre�tractable proboscis and introvert are also found in var�ious groups of Cambrian cephalorhynchs, xenusians,and anomalocaridids (Hou et al., 2006; Gamez Vin�taned et al., 2011; Zhuravlev et al., 2011b); in the lat�ter, the mouth cone is triradiate (Daley and Edge�combe, 2014).

Modern data on the ontogeny of onychophoransshow that the larval mouth begins as terminal, whereasthe antennae and jaws develop from incipient legs andthe jaws are homologous to terminal claws. Theappendages also give rise to slime papillae, which arerevealed by the presence of transient nephridialanlagen (nephridia are absent in adults). The excretorychannels of these nephridia at the antenna and jawbase are closed, although they retain ciliated epithe�lium, and these are transformed into slime glands inthe pair of slime papillae (Eriksson et al., 2003; Mayerand Koch, 2005; Strausfeld et al., 2006). The mouthdevelopment in adults and the initial growth and pri�



mary innervation of the antenna remain unresolved.Some authors studying onychophoran embryogenesisconsider that the ventral mouth in onychophorans isembryologically terminal and that the antennaedevelop from legs and are innervated by the protocer�ebrum (Eriksson et al., 2003). Others think that themouth is formed anew by shifting derivative labialpapillae of the antennae, jaw, and third segments,whereas the antennae are innervated by deuterocere�brum (Ou et al., 2012b). Martin and Mayer (2014)showed that onychophoran antennae are innervatedby the protocerebrum and are hence homologous tothe crustacean labrum, which starts as a paired organas a result of the expression of the regulatory Distal�less gene (Browne et al., 2005; Kimm and Prpic,2006).

Based on the onychophoran ontogeny, the ances�tral taxon of this group can be interpreted as a vermi�form organism with paired retractable undifferenti�ated lobopodia and proboscis and with a terminalmouth. Such organisms present as one of the commonCambrian ecdysozoan groups, which are assigned toXenusia, Tardipolypoda, or simply animals withlobopodia (Dzik and Krumbiegel, 1989; Budd, 1998;Gamez Vintaned et al., 2011; Ou et al., 2012b). Thisgroup includes the famous Hallucigenia, which wasoriginally described upside down and back to front; infact the paired spines are on the back, whereas theflexible appendages are paired walking limbs.

However, xenusians include species with a retract�able proboscis, as in cephalorhynchs, and withappendages clearly unsuitable for locomotion but suit�able for anchoring in holes (Mureropodia) (GamezVintaned et al., 2011) (Fig. 2b), burrowing organisms(Facivermis) with anterior lobodia�like appendagesand a vermiform posterior region (Liu et al., 2006). Inother words the posterior body and caudal segments inthese animals were identical to those in Palaeoscole�cida (earliest cephalorhynchs). Palaeoscolecida wereabundant in the Cambrian and became extinct in theSilurian and were different from other cephalorhynchsin the phosphatized cuticle composed of plates orga�nized in repeating transverse rows similarly morpho�logically organized and structured to those in xenu�sians (and onychophorans, although in the latter thecuticle is not phosphatized). Some Palaeoscolecidaretained reduced paired lobopodia on the ventral sur�face, which probably became sensory glands (tubulesand papillae) as in extant priapulids (Müller and Hinz�Schallreuter, 1993; Zhang and Pratt, 1996; Zhuravlevet al., 2011b) (Fig. 2a).

Cephalorhynchs with priapulid characters begin tooccur in deposits 520 Ma (nearer the end of the EarlyCambrian) (Fig. 1). Many authors still refer to all fossilcephalorhynchs as “priapulids,” although they have acompletely different cuticle and mouth apparatus;these taxa include gigantic animals with a mouth morethan 0.2 m in diameter (Omnidens).

At present they are assigned to several extinctclasses of cephalorhynchs that differ in the head regionmorphology (introvert or non�retractable proboscis),the presence or absence of the neck, and the morphol�ogy of the sensory glands (Conway Morris and Robi�son, 1986; Malakhov and Andrianov, 1995; Hou et al.,2006; Maas et al., 2007; Harvey et al., 2010; Zhuravlevet al., 2011b; Liu et al., 2014). There are confirmedrecords of burrows of Cambrian cephalorhynchs con�taining buried remains of inhabitants that are some�times identifiable by species (Zhang et al., 2006;Zhuravlev et al., 2011b; Huang et al., 2014): these aresimple U�shaped burrows (Fig. 2a) or dead�end, sac�like burrows similar to those inhabited by extant pri�apulids and completely unlike false traces Treptichnuspedum common in the basal Cambrian, which havebeen interpreted as priapulid burrows (Vannier et al.,2010). Thus, there is no evidence suggesting thatcephalorhynchs preceded xenusians. The latter areknown from beds over 525 Ma as larval skins (Xenu�sion; Dzik and Krumbiegel, 1989) and from beds olderthan 535 Ma as phosphatized claws and cuticularspines, whereas the first confirmed cephalorhynchs(Palaeoscolecida) appeared no earlier than 525 Ma(Zhuravlev et al., 2011b; Caron et al., 2013b). The lar�vae of priapulids, loriciferans, and nematophorans,and even their adults, retain characters of palaeoscole�cids and their larvae in the structure of the cuticle(Maas et al., 2009; Peel, 2010). Kinorhynchs,although not found as fossils, have a serial arrange�ment of muscle facies associated with the cuticularsegments and a mouth cone like that in Cambriancephalorhynchs (Omnidens). Reverse evolution—from cephalorhynchs to xenusians and arthropods—isadhered to by almost all authors (Dzik and Krumbie�gel, 1989; Budd and 2001; Zhang and Briggs, 2007;Daley et al., 2009; Liu et al., 2011; Legg et al., 2013)and is just a reworking of the annelid�arthropodhypothesis. The transformation of a highly specializedintrovert into the simple mouth of xenusians and of thesensory glands (papillae) into the locomotory append�ages of cephalorhynchs, which needed to be able toescape somehow from their burrows onto the sub�strate, is impossible biomechanically: the locomotionof such worms by hydraulic pumping and coelomicfluid distribution is only suitable to move within thesubstrate. The evolution from worms with a retractableproboscis to onychophoran�like organisms is not inagreement with the data on the brain ontogeny in ony�chophorans: it has been shown that their brain is not ofcircumpharyngeal origin (Eriksson et al., 2003) butbegins as paired dorsal ganglia, the protocerebral partof which innervates the antennae and eyes and thedeuterocerebral part innervates the jaws, whereas thetritocerebrum is not formed (Strausfeld et al., 2006;Martin and Mayer, 2014). Based on the presence ofantennae and eyes in some xenusians, it is possible tosuggest that the brain of xenusians with a nonretract�able proboscis was similar.

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Xenusians represent a stem group not only forcephalorhynchs and onychophorans. Tardigrades arealso their possible descendants; they are adapted tomeiobenthic habitats and thus have acquired a simpli�fied system of inner organs while retaining the initialmorphology of lobopod�like appendages with clawsand cuticle. Tardigrades stylets are derivatives of thelobopod�like limbs that were transformed into innerorgans (Dewel and Eibye�Jacobsen, 2006; Halberget al., 2009), resulting in the bilateral appearance oftriradiate mouth apparatus. The transformation of themuscles from one complex of longitudinal and trans�verse muscles to the serial fascia, which connects thelimb to the cover plates, is observed in the Cambrianxenusians Hadranax and Pambdelurion (Budd, 1998,2001) (Fig. 2f), whereas the earliest Middle Cambriantardigrade has paired rudiments of the lobopodianappendages in the head region, in addition to fourpairs of locomotory limbs and Cuticular plates likethose in xenusians (Maas and Waloszek, 2001). Thisprocess is connected with the functional differentia�tion of limbs and apparently with the transformationof the ventral nervous cords into the segmented andlater ganglionized ventral chain (Whittington andMayer, 2011).

Another group likely to be associated in its originwith xenusians—anomalocaridids (Anomalocaris,Peytoia, Amplectobelua, and others)—are the largestinhabitants of the Cambrian seas, up to one meter long(Figs. 2g and 2i). They have a proboscis with radiallyarranged tooth plates, sometimes of several orders, asin cephalorhynchs (radiodonts or dinocarids); a pre�oral pair of segmented or lobopod�like lobe graspingappendages, as in some xenusians; large compoundeyes (up to five in number), similar to the opticalorgans of the most derived arthropods; a head shieldsometimes composed of several elements; a body withswimming lobes possibly bearing respiratory fila�ments; and a caudal region with or without cerca anda straight gut with serial paired digestive diverticulae(Whittington and Briggs, 1985; Hou et al., 2006;Zhang and Briggs, 2007; Daley et al., 2009; Patersonet al., 2011; Daley and Edgecombe, 2014). This groupalso accommodates Opabinia and Nectocaris, whichhad been erroneously considered to be the earliestcephalopod, and chordates with a head shield, oralproboscis, paired preoral appendages, and external gillfilaments (Fig. 2h). Anomalocaridids with preoralappendages, which were most likely to be innervatedfrom the protocerebrum, can be considered descen�dants of xenusians that adapted to nektobenthic activepredation and active filtration, based on the mouthapparatus and in some taxa (Kerygmachela and Tami�siocaris), the pre�oral lobopod appendages (Bergströmand Hou, 2003; Hou et al., 2006; Daley and Peel,2010).

It does not seem correct to consider anomalocari�dids, which were extinct in the Devonian Period, asthe basal group for arthropods, as is considered in the

cladograms in which they are placed between xenu�sians and true arthropods (Euarthropoda) (Budd andTelford, 2009). First, they lack the definitive charac�ters of arthropods, apart from the preoral—append�ages that are not always segmented and compoundeyes. Second, the mosaic combination of characters invarious species of anomalocaridids and xenusianscrushes all cladistic schemes. For example, amongxenusians, Diania have strongly cuticularized, almostsegmented appendages and a head region withouttraces of a tagmosis and with a well�developed probos�cis (Liu et al., 2011; Ma et al., 2014) (Fig. 2d). On thecontrary, Antennacanthopodia had lobopod�likeappendages with claws and a head region with traces oftagmosis and a reduced proboscis (Ou et al., 2011)(Fig. 2e), whereas Mureropodia has an introvert andreduced lobopod�like appendages with claws(Zhuravlev et al., 2011b) (Fig. 2b). Arthrodization andarthropodization did not necessarily occur togetherbut instead developed independently in several groupsof Ecdysozoa (Ponomarenko, 2008; Mounce andWills, 2011): xenusians, anomalocaridids, vetulico�lians, and partly tardigrades.

Kinorhynchs are worth mentioning again(Schmidt�Rhaesa and Rothe, 2006). The origin ofPycnogonida is not certain (whether they are truearthropods, closely related to chelicerates, or acquireda segmented skeleton independently), because fossilCambrian and Jurassic taxa have features of organiza�tion of the head section like those in xenusians(Waloszek and Dunlop, 2002; Charbonnier et al.,2007). The Early Cambrian arthropods Fuxianhuiaand similar taxa had the most simple plan of the headregion but with true antennae, a second specializedpair of segmented appendages and differentiation ofthe ventral somite into sternites and tergites, undiffer�entiated cylindrical walking limbs with numeroussmooth podomeres, and a rounded distal segment(Chen et al., 1995b; Bergström et al., 2009; Ma et al.,2012; Tanaka et al., 2013; Yang et al., 2013), differingfrom the lobopod�like appendages in the higher degreeof sclerotization, approximately as in Diania Xenusia(Fig. 1).

The presence of the coelom in arthropods and ony�chophorans does not contradict the original positionof xenusians as the ancestral group of Ecdysozoa,including cephalorhynchs (Eriksson et al., 2003;Schmidt�Raesa, 2006), because a reduced coelomnear the anterior gut is found also in priapulids (Meio�priapulus; Storch et al., 1989). Apart from that, thedistinct axial position of the gut in xenusians,palaeoscolecids, and some other Cambrian cephalo�rhynchs suggest the presence of a controlling structurethat is similar to the mesentherium and hence thecoelomic cavity (Zhuravlev et al., 2011b).

Whether or not Articulata is a “natural ” group, thelabrum of arthropods develops as a paired organ ratherthan the homologous prostomium of annelids (Melni�kov, 1970; Melnikov et al., 1992; Kimm and Prpic,



2006), whereas the paired ventral nervous chains inthese two groups have different origins and are nothomologous to one another if the nervous system ofonychophorans with ventral cords lacking ganglia andaggregations of gangliose cells is considered to be astem group for arthropods (Mayer and Harzsch, 2007;Whittington and Mayer, 2011). The similarity of bothgroups appears to be determined by the fact thatarthropods, representing Ecdysozoa, and annelids,representing Lophotrochozoa, retained a certain set ofcharacters of the common ancestor of Bilateria,including the limbs (Balavoine and Adoutte, 2003;Prpic, 2008; Williams et al., 2012).

Nielsen (2003), who tried to retain a united Artic�ulata (Annelida + Arthropoda) (to which he had toassign Cycloneuralia with kinorhynch (also cephalo�rhynchs), like the intermediate change betweenarthropods and priapulids–nematodes), considers thetrochophore larva with a preoral crown of cilia (pro�totroch) a synapomorphy of all protostomes and alsonoted its clear absence in arthropods and cycloneura�lians, i.e., in all Ecdysozoa(!). However, if the inter�mediate forms between different groups of Ecdysozoain the fossil record are found in abundance, someforms, which could have been considered intermedi�ate between annelids and arthropods, are completelyabsent in the beds (for example, if anomalocarididswith a proboscis slightly resembling the axial pharynxof some polychaetes were considered as such interme�diate forms, their swimming lobes would have retainedthe supportive setae necessary for the attachment ofmuscle bunches of the locomotory system. Why wouldthey then need to switch to an external attachment ofthe same musculature to the external carapace?)

Lophotrochoans:the only Skeletons in the Closet

Annelids, or, more precisely, imprints of their cov�ers, are also found in the Cambrian beds, althoughthey are a thousand times less common than cephalo�rhynchs. They are exclusively represented by theremains of motile polychaetes with bifurcate parapo�dia (noto� and neuropodia) (Conway Morris, 1979;Conway Morris and Peel, 2008; Vinther et al., 2011)(Fig. 1); only one, not the earliest, annelid taxon, Per�ochaeta, with thick, hook�like setae was probably notparticularly motile (Merz and Woodin, 2006). None ofthe Cambrian annelids with their combination ofcharacters can be assigned to any extant group: theylack antennae, supporting chaetae, and dorsal or ven�tral setae, and the palps are very simple (Eibye�Jacob�sen, 2004; Eibye�Jacobsen and Vinther, 2012). Scole�codonts (fossil jaws of polychaetes) appear only in theOrdovician beds, whereas reliable Sedentariaappeared in the Mesozoic (tubes with a microstructurecharacteristic of annelids are found beginning fromthe Triassic (Vinn, 2006; Vinn et al., 2008; Vinn andMutvei, 2009).

Imprints of earlier annelids, such as Protoarenicolafrom the Cryogenic and Ediacaran beds of NorthChina, were in fact remains of algae with siphonateorganization (their carbonized covers had the samestructure as associated algal thalli, while the “retract�able pharynx” was the attachment disc (Dong et al.,2008; Butterfeld, 2009).

On the whole the fossil record of early annelids isa good illustration of Westheide’s (1997) theory of theorigin of chaetae as external defense elements inmotile epibenthic taxa. The first polychaetes, e.g.,Canadia, had exactly this “horrent” look. Later, asworm�like locomotion developed, the covers devel�oped transverse gaps lacking chaetae determining theexistence of external metamery. Struck et al. (2011)and Struck (2013) studied the molecular phylogenet�ics of annelids and noted that this group includes twodistinct branches, Errantia and Sedentaria. The com�mon ancestor of all annelids in these authors’ recon�struction is a motile�segmented animal with devel�oped parapodia on metameres along the entire body(Struck et al., 2011, fig. 2).

Other worms belonging to Lophotrochozoa are notfound in the Cambrian. Although Archaeogolfigia andCambrosipunculus from Chengjiang (Huang et al.,2004) have already been suggested as representatives ofthe terminal group of sipunculids, which Eibye�Jacobsen and Vinther (2012) thought to be sufficientevidence to reconsider the new system of annelids, wasproposed by Struck et al. However, the fossils them�selves do not provide sufficient evidence for either the�ory: it is not certain that tentacles were present in atleast one of four specimens in both genera, and the gutdoes not show undulation curves characteristic ofsipunculids. Moreover, the body surface of theseworms clearly shows scalides and sclerites like those inpalaeoscolescids, and are also abundantly found in thesame bed in Chengjiang. The straight, “posterior” sec�tion of the gut is in fact imprints of the retractory mus�cles of the introvert structures found in Palaeolescidae(Zhuravlev et al., 2011b). The literature on the Edi�acaran and Cambrian period still has references to theoccurrence of Pogonophora. In fact these are ribbedorganic tubes of problematic sabelliditids, the micro�structure of which is distinct from that of Pogono�phora (Urbanek and Mierzejewska, 1983; Ivantsov,1990).

It is interesting that, among the Ordovician–Car�boniferous annelids crawling on the surface of the sub�strate, there were segmented taxa with calcareouselytra (Machaeridia) covering the parapodia with cha�eta (Vinther et al., 2008; Vinther and Briggs, 2009).The elytra of Machaeridia are similar to the shells ofPolyplacophora and diverse Cambrian “polyvalves”(Fig. 4e). It is not surprising that they were recentlyassigned to mollusks and to aplacophorans, which isstrongly supported by cladistics analysis (Sigwart andSutton, 2007).

Diverse polyvalved taxa (Halwaxiida or Halkieri�idae) are most interesting from the point of view of the

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origin of mollusks and other Lophotrochozoa. Theyare united with Siphogonuchitidae in the orderSachitida and with the order Chancelloriida in theclass Coeloscleritophora (Bengtson and Missar�zhevsky, 1981). The complex external skeleton, orscleritome, of these organisms, which developed onthe dorsal and lateral sides, is composed of numerouscalcareous and/or organic sclerites and spicules of var�ious shapes and one–two shells on the anterior andposterior ends of the body resembling shells of brachi�opods or monoplacophorans (Fig. 4c). Apart from theabove groups, Coeloscleritophora apparently includeMaikhanella and other Maikhanellidae, the cup�likeshells of which consist of fused sclerites very similar tothose of siphogonuchitids (Bengtson, 1992). The posi�tion of all of these fossils within Lophotrochozoa andtheir affinity to Wiwaxia, which has the organic scleri�tome, is debatable. Some authors compared the largeshells with those of brachiopods and other scleriteswith the elytra and chaeta of annelids, consideringhalkieriids and halwaxiids to be stem groups ofLophotrochozoa as a whole (Conway Morris and Peel,1995; Holmer et al., 2002; Conway Morris and Caron,2007). Other authors, based on data on the scleritestructure (i.e., the presence of a complex system ofcanals connecting the interior cavity of a sclerite withits surface, that is indistinct from the canals penetrat�ing chiton shells and housing the epithelial papillae(estetes) and the mouth apparatus, which resembleradula), consider them to be true mollusks precedingpoly� and aplacophorans (Scheltema and Ivanov,2002; Vinther and Nielsen, 2005; Vinther, 2009;Smith, 2012). Interestingly, even the hardest elementsof the same scleritomes, if their mineral composition iscompletely dissolved, show capillaries, as in the chae�tae of the synchronous annelids, e.g., Canadia (But�terfeld, 1990, 2003, 2006). However, it is impossible tosimultaneously accept these chaetae as a synapomor�phy of Lophotrochozoa or to consider their presenceas exclusive to annelids, as is thought by some authors(Eibye�Jacobsen, 2004).

Chancelloriidae complicates (or clarifies) the situ�ation even more. Sclerites of this group are assembledin rosettes with one hollow central spine and three ormore strongly peripheral ones. The microstructure ofthese sclerites and general body plan (a hollow, thin�walled, elongated sclerite with a distinct basal fora�men) is identical to that of halkieriids and other celo�scleritophorans (Butterfeld and Nicholas, 1996;Ivantsov et al., 2005; Porter, 2008). They formeda completely different structure—a hemispherical ornarrowly conical scleritome with a cavity opening atthe top (Fig. 4d). Therefore, Chancelloriida were fora long time considered to be sponges similar to heter�actiniids. The lower ends of these organisms wereattached to the substrate, supported by the occur�rences of complete scleritomes of Chancelloriida inthe Lagerstätten and reef limestones, where they wereburied in the lifelike position (Zhuravlev, 2001a).Chancelloriida imprints show a nonporous bilayered

integument, with the outer tuberculate layer mineral�ized in the places of sclerite development and the innerunderlying it and filling in the canals in the sclerites(Bengtson and Hou, 2001; Janussen et al., 2002).

Cambrian sclerites of “polyvalves,” includingchancelloriids, typically with a thin inner organic layerand a relatively thick middle layer, are composed ofprimary aragonite fibers oriented along the axis of thesclerite at a small angle to its surface, which deter�mined the scale�like ornamentation of the surface,and a thin external organic cover. The mineral layercan be penetrated by canals (Butterfeld and Nicholas,1996; Porter, 2008; Vinther, 2009). This microstruc�ture selection has no equivalent in true mollusks, butsome features of the cross�laminated microstructureand scale�like ornamentation (apparently calcifiedperiostracum) in the shells of Maikhanellidae, whichcould be part of the scleritomes (they are only absentin Chancelloriidae), also point to the similarity of thisgroup to Mollusca, whereas the cap�like protoconch issimilar to that of monoplacophorans (Feng et al.,2003; Ponder et al., 2007).

Interpretations of the earliest cap�like and coiledCambrian shells essentially varied; although they wereassigned to monoplacophorans (Runnegar and Jell,1976; Runnegar, 1996), gastropods (Golikov and Star�obogatov, 1988) and to the extinct classes Helcionel�loida and Paragastropoda, and occasionally to Rostro�conchia (Pojeta and Runnegar, 1976; Linsley andKier, 1984; Peel, 1991), there was no doubt that thesewere indeed mollusks. Yochelson (1975, 1978) sug�gested that such shells could belong to worms, but atthat time neither the microstructure, nor protoconchsor muscle scars on these shells had been studied, andtheir general morphology was poorly described.

Parkhaev (2004, 2008, 2014) and Ushatinskaya andParkhaev (2005), based on Parkhaev’s collection ofancient fossil mollusks, which is the largest in theworld, studied the muscle scars, microstructure, andprotoconch with a septum separating it from theteleconch and concluded that most of these animalswere primitive endogastrically coiled gastropods,which he separated into the class Archaeobranchia.The first members of the more derived gastropod sub�classes Divasibranchia (Khairkhaniidae) and Dextra�branchia (Onychochilidae) (Parkhaev, 2008) simulta�neously appeared in the Early Cambrian. The earliesttaxa include true bivalves (Vendrasco et al., 2011), theearly separation of which within the shelled mollusksis supported by the analysis of the complete mitochon�drial genome (Plazzi et al., 2013).

The microstructure of many shells of extinct andextant mollusks certainly has certain equivalentsamong the microstructures of brachiopod shells andbryozoan skeletons, because they all represent theclade Lophotrochozoa (the microstructural similarityof shells of mollusks, brachiopods, and bryozoans is agood synapomorphy for this clade, which has so farrarely been mentioned in papers). In addition, Cam�brian mollusk shells have cross�laminate, lamello�



fiber, scale�like calcitic and aragonitic and other typesof microstructures found in mollusks; the differencebetween the Cambrian and later taxa is that newmicrostructures appeared in the course of the molluskevolution, including the nacre sensu stricto structure(Checa et al., 2009; Vendrasco et al., 2010, 2011,2013). The appearance of new microstructure typesthat better resist mechanical stress was caused by anincrease in the diversity of predators and their ability tobreak into the shells (Vermeij, 1990; Wood andZhuravlev, 2012; Vendrasco et al., 2013).

The cap�like shells do indeed belong mainly toancient mollusks, i.e., ancestral taxa that gave rise tothe Later Cambrian–Ordovician radiation of gastro�pods, scaphopods, polyplacophorans, and cephalo�pods (Zhuravlev, 2001). Throughout their evolutionvarious Bilateria retained the original mineral compo�sition of their shell, which was formed in an equilib�rium with the environment: animals that appeared inthe cold “aragonite” eras had aragonite or high mag�nesium shells, and those that acquired a mineral skel�eton in warm “calcite” eras have shells with a highmagnesium�calcite composition (Wilkinson, 1979;Zhuravlev and Wood, 2008; Porter, 2010). The alter�nation of “aragonite” and “calcite” eras dependedmainly on the hydrothermal regime, which influencedthe proportions of Ma and Ca ions in the ocean, andthe partial pressure of carbon dioxide, which affectedthe kinetics of the crystal growth determining theirshape (the crystalline structures of calcite and arago�nite are different (Sandberg, 1983; Stanley and Har�die, 1999; Morse et al., 2006)).

The shell of the earliest known cephalopod Plec�tronoceras is aragonitic (Landing and Kröger, 2009),although the time of its appearance coincided with the“calcite” era. This means that this taxon certainly hadEarly Cambrian ancestors with an external aragoniticshell. The most recent studies of Nautilus and coleoidsshowed that they share their ontogentic mode withgastropods: the embryonic organs form a concentricarrangement around the antero�posterior axis, with ashell plate on the dorsal side (even in shortfin squidwith an almost reduced skeleton), whereas the funnel,which is part of the mantle fold, is formed at the pos�terior end of the embryo and turns toward the headwith growth. In coleoids the embryonic shell is gradu�ally shifted within (Shigeno et al., 2008; Kröger et al.,2011). Plectronoceras and some of the other earliestcephalopods retain a number of primitive features inadults, i.e., the shell was dorsal and the funnel was pos�teriorly positioned, while the paired muscle scarsresemble those in monoplacophorans (Mutvei et al.,2007; Kroger et al., 2011). In addition, Plectronocerasand the majority of the earliest cephalopods lack aprotoconch, suggesting that they evolved from benthicancestors. Presumably, the protoconch appeared laterand independently in different lineages of cephalo�pods that became planktonic (Barskov, 2012). It is notsurprising that the most comprehensive molecularstudies of 1185 mollusk genome regions performed in

a sample of 15 species and together with previous datarepresenting all classes, including newly obtainedmonoplacophorans, revealed that monoplacophoransare a sister group of cephalopods within Conchifera,whereas scaphopods, gastropods, and bivalves forma second clade (Smith et al., 2011). Another recentmolecular tree, in which Cephalopoda and Aculifera(Aplacophora + Polyplacophora) are sister groups(Vinther et al., 2012), was built by sequencing sevennuclear genes in 14 species of mollusks, but it did notinclude monoplacophorans. Finally, another molecu�lar tree connecting polyplacophorans and monopla�cophorans (clade Serialia) was built based on the DNAof a monoplacophora specimen; the DNA highlydegraded probably because of bulk fixation of the sed�iment on the vessel (Giribet et al., 2006). Thus, mor�phological, ontogenetic, and paleontological datasupport the hypothesis of cephalopod origin frommotile Early Cambrian mollusks with an external shellrather than from some sedentary clonal organisms orsoft�bodied nektonic animals. At least 30 Myr passedbetween the appearance of the cap�like gastropods andmonoplacophorans and the appearance of cephalo�pods, which is sufficient for this evolution.

The occurrence in Herefordshire of Silurian mol�lusks (Acaenoplax, Kulindroplax, and others), whichcombine characters of polyplacophorans (several rowsof calcareous dorsal plates) and aplacophorans (man�tle groove along the ventral side, or completelyreduced foot), support the hypothesis of aplacoph�orans having evolved from Cambrian polyplacoph�orans with calcareous sclerites and a normally devel�oped foot (Sutton et al., 2001, 2012) (Fig. 1). This sce�nario is repeated in the embryogenesis ofaplacophorans, at least in Caudofoveata (Scheltemaand Ivanov, 2002; Nielsen et al., 2007).

While the earliest mollusks, except for Chancellor�iidae, and annelids were exclusively motile taxa, thesituation was different among the earliest tentacledanimals. These mainly include sedentary forms withdifferent numbers of valves: from two (as in typicalbrachiopods of all three subphyla: Linguliformea (for�merly inarticulate brachiopods with a phosphateshell), Craniiformea (inarticulate brachiopods with acalcareous shell), and Rhynchonelliformea (remain�ing inarticulate and articulate brachiopods with a cal�careous shell)) up to 30 or more (as in Paterimitra andEccentrotheca) belong to the extinct group Tommoti�ida discovered in Siberia (Missarzhevsky, 1989). InEccentrotheca, one of the earliest tommotiids, thephosphate porous shells (sclerites) were of two types:irregular cap�like and flattened. The sclerites werearranged spirally and formed a narrow conical externalskeleton 4�mm tall, open at top and bottom (Skovstedet al., 2011). The scleritome of Paterimitra was gener�ally similar to that of Eccentrotheca, but had threetypes of sclerites, two of which resembled shells of bra�chiopods (Skovsted et al., 2009c) (Fig. 4a). The simi�larity with brachiopods is emphasized by the identicalmicrostructure with large cavities between the layers of

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shell, microornamentation with a characteristic retic�ulate surface, and the presence of pores with imprintsof setae (seta are sometimes present due to phosphati�zation), which allows tommotiids to be considered astem group for brachiopods, whereas the earliest shellsof brachiopods (Aldanotreta, Askepasma, and Salany�golina from the class Paterinata) have a microstructureof the tommotiid type (Bengtson, 1970; Holmer et al.,2008b, 2009; Skovsted et al., 2009c, 2011; Topperet al., 2013a). The bivalivian tommotiids Micrina andTannuolina, with a few sclerites, are particularly inter�esting as possible transitional forms (Fonin andSmirnova, 1967; Laurie, 1986): Micrina has an embry�onic shell, a bivalvian protegulum with seta sockets.The protegulum in brachiopod embryos is formedbefore hatching, and one protegulum valve in Micrinapossesses a cross�folded posterior projection similar tothe analogous structure in the Cambrian brachiopodMickwitzia and other Lingulata and suggesting thepresence of the embryonic pedicle (Balthasar, 2004;Holmer et al., 2008a, 2011; Balthasar et al., 2009;Skovsted et al., 2009b).

Presumably, Linguliformea and Rhynchonelli�formea could have independently evolved by paedo�morphosis from a bivalvian larva of some tommotiids(Holmer et al., 2011; Skovsted et al., 2011). Moreover,different classes of Linguliformea could have evolvedfrom different tommotiids: Paterinata, from Eccen�trotheca and Lingulata, from Tannuolina�Micrina(Larsson et al., 2014). In general, early brachiopodsshow an interesting mosaic pattern: the shells of mostmembers of ancient classes, including Chileata, Obo�lellata, Kutorginata, and Paterinata, which becameextinct in the Cambrian or in the early Paleozoic,combine morphological and microstructural charac�teristics of Linguliformea and Rhynchonelliformea(Ushatinskaya, 1987, 1998; Popov et al., 1996; Williamset al., 1996; Malakhovskaya, 2008; Balthasar, 2008;Holmer et al., 2009; Zhang et al., 2011) (Fig. 1). Thedifferences between the Cambrian and extant brachi�opods deepened due to the discovery of a fossil brachi�opod with preserved shell interior, including the pedi�cle, visceral cavity, and the lophophore. It has becomeevident that, while the shells of the extant and fossilLingulata were superficially similar, their interior wasvery different, whereas the position of the pedicle andthe morphology of the lophophore in many Cambrianbrachiopods have no equivalents among extant brachi�opods; for instance, in large, freely lying Heliomedusa,two wide semicircles of dense ciliate setae projectbeyond the shell, as in the larvae of extant Lingula orGlottidia (Zhang et al., 2004, 2009, 2011).

Interestingly, two groups of tommotiids, eachincluding one genus (Camenella and Sunnaginia),have dense layers of nonporous paired (mirror sym�metrical) sclerites, which were probably arranged onthe surface of the bilaterally symmetrical animals(Skovsted et al., 2009a; Murdock et al., 2012)(Fig. 4b). This means that the earliest Lophotro�chozoa were not exclusively sedentary filter�feeders

but also included motile epibenthic detritus feeders(otherwise, why would they need a protective cover?).It is not certain whether these gave rise to some extanttentacled Lophotrochozoa or disappeared altogetherlike Chancelloriidae, the only known extinct sessilemollusk�like group?

The discovery of a complete scleritome of halkieri�ids suggested that these free�moving organisms couldbe ancestral to brachiopods, which became sessileonly later and lost all sclerites, except for the two larg�est ones that gave rise to the bivalvian shell coveringthe dorsal and ventral sides (Nielsen, 1991; Cohen etal., 2003; Malakhov, 2010). However, the most recentdata on the embryogenesis of Novocrania anomala(Craniiformea) revealed that its larva lies on the ven�tral side during metamorphosis, anchored by the endof the posterior larval lobe, which is curved onto theventral side, whereas the anterior larval lobe forms adorsal mantle lobe and secretes the dorsal valve. Thedevelopment of the ventral valve is delayed, and it isfinally formed by the ventral mantle lobe (Altenburgeret al., 2013). Brachiopods preserved in Lagerstättenhave their gut preserved, demonstrating that this organwas U�shaped in different groups (Zhang et al., 2004,2009), and, as is suggested by paleontological evi�dence, brachiopods could have evolved from sessiletommotiids, which represent the archaic groupLophotrochozoa.

Sessile tubular tommotiids, like Eccentrotheca, arethought to be ancestral to phoronids (Skovsted et al.,2011). Balthasar and Butterfeld (2009) proposed a dif�ferent pathway for phoronid evolution, from Cam�brian brachiopods with a nonmineralized, chitin shell,like Lingulosacculina, through the miniaturization ofthe organs, which in phoronids are similar to those inbrachiopods: dermal muscles and U�shaped gut; lat�eral mesenteries bearing gonads; posterior projectionof the coelomic cavity, which was used for anchoringin the substrate. However, all of these organs arestrongly diminished, while setae are absent. Bryozoanscan also be derived from the basic brachiopod�likebody plan as clonal modular descendants of tommoti�ids that lost the phosphatic skeleton: abundant pri�mary phosphatic taxa existed at the beginning of theEarly Cambrian, when the oceans containedincreased quantities of phosphate (Cook and Sher�gold, 1984).

However, bryozoans first appeared in the LateCambrian and had skeletons of low�magnesium cal�cite characteristic of this period (Landing et al., 2010),which could indicate their origin from a soft�bodiedtaxon. Molecular data suggest that brachiopods,phoronids, and bryozoans are related within Lopho�phorata, which suggests homology of their lopho�phores despite some small differences (Nesnidal et al.,2013).

Cotyledion from Chengjiang of China, another rep�resentative of the Early Cambrian Lophotrochozoawith a weakly phosphatized scleritome, has a flexiblestalk, a calyx, a U�shaped gut with a slit�like mouth,



and an aboral anus ringed by 30 marginal tentacles.This fossil is externally similar to Kamptozoa (Zhanget al., 2013) (Fig. 1). However, it is significantly largerthan any extant kamptozoan (5.5 cm instead of 1 cm),and the calyx is covered by rounded sclerites. Theauthors who described this species assume that kamp�tozoans could have evolved through miniaturizationand simplification of the primary organ set in largerorganisms. The sclerites resemble mobergellans,phosphate rounded layered shells slightly resemblinglarval brachiopod shells.

Cambrian Lophotrochozoa include another threerepresentatives groups: hyoliths, which survived untilthe Permian in a much more impoverished state thanin the Cambrian, Early–Middle Cambrian stenothe�coids, and Early Cambrian siphonoconchs. Hyolithsand stenothecoids, based on the shell microstructure,were more closely related to mollusks (Kouchinsky,2000; Feng et al., 2001; Martí Mus and Bergstrom,2007; Zhuravlev and Wood, 2008), but they consider�ably differed from the latter in the general body planand were even recognized as the independent phylaHyolitha and Stenothecata (Runnegar et al., 1975;Sysoev, 1976; Rozov, 1984). The shell in true hyolithswas composed of a large conical valve and an opercu�lum, with two logarithmically coiled supports (helens)sealed with the operculum. In light of the complex sys�tem of muscle scars on the operculum, it served notonly for the tight closure of the shell by slightly retract�ing in the conical valve but also for controlling themuscles of the appendages. The combination of theoperculum and appendages exclude the presence of amuscle foot in hyoliths. They probably just lay on thesubstrate, supported by the appendages, and couldonly change position slightly in the direction of thebottom currents in order to catch suspended particlesusing the mantle trail or a lophophore�like structure,which is suggested by occurrences of oriented shells ofhyoliths in living position on bedding planes (Kruseet al., 1995). Other hyoliths, Orthothecida, lackappendages and are commonly found buried vertically.Sometimes adult orthothecids have their gut preserveddue to phosphatization. The gut is composed ofstraight (anterior) and folded (posterior) regions, as insipunculids; whereas both region of the gut are straightin hyoliths and juvenile orthothecids (Devaere et al.,2014). Stenothecida were bivalvian organisms thatsuperficially resemble brachiopods more than bivalvesbut have serial paired muscle scars as in monopla�cophorans. The third, less well known, group of Cam�brian lophotrochozoan “bivalves” is the classSiphonoconcha, or Tianzhushanellidae: their symme�try resembles that of brachiopods but with one valvewith ear�like extensions on the area and a valve with asiphonal groove articulated with dental apparatus(Parkhaev, 1998). All of these groups apparently repre�sent an early radiation of Lophotrochozoa.

Extant Lophotrochozoa in general retained a fewsynapomorhies. One of the most important synapo�morphies is the spiral determinate cleavage with sepa�

rate micromere 4d, appearing at the stage of 64 cells,which later evenly divides to form the incipient bilat�erally symmetrical mesoderm (annelids, sipunculids,echiurids, myzostomids, nemerteans, camptozoans,phoronids, and mollusks; this is lost in brachiopodsand bryozoans, but present in acanthocephalans andplatyhelminths) and planktotrophic larvae (tro�chophore) with a prototroch (pre�oral ciliated band),paired protonephidia, ciliated tuft, and apical plate,which is retracted during metamorphosis into the inte�rior, and to form a brain (annelids, sipunculids, echiu�rids, myzostomids, camptozoans, phoronids, bryozo�ans, cycliophoran, and mollusks; in nemerteans andbrachiopods there are only cell homologues of the pro�totroch; the trochophore is considered to have beenlost in cephalopods mollusks and clitellates) (Funch,1996; Rouse, 1999; Maslakova et al., 2004; Lambert,2010; Meyer et al., 2010; Gline et al., 2011; Penner�storfer and Scholz, 2012). Synapomorphies ofLophotrochozoa in the fossil record include the skele�tal microstructure discussed above and chitinous(β� or γ�chitin) chetae secreted in sac�like invagina�tions of the cuticle by large epithelial cells (chaeto�blasts) with microvilli capillary�shaped, traces ofwhich remain (annelids, myzostomids, brachiopods,polyplacophorans, and juvenile cephalopods, as wellas bryozoans, in which chitinous teeth in the stomachare homologous to chetae) (Eibye�Jacobsen, 2004;Giribet et al., 2009).

And Many Others

The Cambrian also yields remains of chaetognathsand ctenophores. The latter are buried only in Lager�stätten and are very similar to extant species in thegeneral body plan, although some have a differentnumber of combs (Conway Morris and Collins, 1996;Chen and Zhou, 1997) (Fig. 1). The most interestingis the discovery of Maotianoascus represented by bothadult and embryonic specimens: this is a radially sym�metrical organism with eight rows of combs lackingtentacles and therefore resembling modern Beroidea(Chen et al., 2007).

Chaetognaths are very rarely found as completeimprints (Chen and Huang, 2002; Vannier et al., 2007)(Fig. 1), but their phosphatized dental apparatus,known as protoconodonts (Protohertzina), is com�monly found beginning from the basal Cambrian.These remains differ from true conodonts and otherchordates in the microstructure, which are character�istic of the skeletal elements secreted on the epithelialsurface rather than in the fold of the epidermis, andthus they are commonly found as paired aggregates ofseveral morphologically uniform denticles (Bengtson,1983; Szaniawski, 2002). The early appearance of cha�etognaths in the fossil record agrees with their positionas a sister group of all protostomes in molecular phy�logenies (Halanych, 2004) and their unique genome(Marlétaz et al., 2008).

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It is unlikely that even the best Cambrian Lager�stätten will produce cycliophores, orthonectids,acoelans, or other groups lacking any hard structures.The fossil record of those that colonized land begins inthe mid�Mesozoic by the appearance of the resin�pro�ducing gymnosperms (in amber). Scientists some�times (with much success) attempt to infer the pres�ence of these organisms from characteristic injuries inthe skeletons of trilobites, crinoids, and other inhabit�ants of ancient seas, but only in those tha became par�asites. However, there are several “unidentifiedobjects,” including calcareous spirally coiled shells ofcribricyaths, conical shells of Solterella with alternat�ing agglutinated and secreted layers, imprints ofmedusoid parapsonemids with a U�shaped gut andtentacles encircling the mouth, and some remainsfrom the Burgess Shales and other Lagerstätten thatcannot be currently placed (Amiskwia, Dinomischus,Odontogriphus, and Oesia) (but these are unlikely toinclude acoelans or acanthocephalans).

Previous discussion shows that Cambrian fossils,including sponges, cnidarians, cephalorhynchs orannelids, arthropods, mollusks, brachiopods, echino�derms, or chordates, let alone tommotiids or chancel�loriids, lack key characteristics occurring in the extantmembers of these clades, and commonly even in theirnearest (Ordovician) descendants. All of these fossilsrepresent ancestral groups or their extinct branches.For instance, new microscopy methods showed that,among Cambrian arthropods, which less than 10 yearsago were thought to be good examples of terminalgroups of crustaceans, i.e., Branchiopoda and Phyl�lopoda (Isoxys, Canadaspis, Rehbachiella), and ostra�codes (bradoriids, phosphatocopids), include notaxon with a set of limbs that would allow its unequiv�ocal assignment to a class of crustaceans or could beidentified with certainty as Mandibulata. They canhave giant grasping appendages instead of antennae ora hypostome connected to the anterior pair of append�ages. Epipodites specialized for breathing or osmoreg�ulation can be completely absent, whereas all headappendages can be totally uniform, indistinguishablefrom the walking limbs, etc. (Stein et al., 2008; Maaset al., 2009; Vannier et al., 2009; Haug et al., 2010,2012; Legg et al., 2012, 2013).

Very interesting data on the organization of the ner�vous system on the earliest arthropods were obtainedby studying the most common Chengjiang fossils(Fuxianhuia and Alalcomenaeus): a combined use ofX�ray computer tomography and fluorescent micros�copy shows the distribution of iron and other chemicalelements in clay minerals replacing the soft tissues,thereby showing a very fine detail of the nervous sys�tem up to the optical nerve and nervous fibers leadingfrom various parts of the brain to the limbs (Ma et al.,2012; Tanaka et al., 2013). It was demonstrated thatFuxianhuia, which has been treated in all phylogenetictrees as a basal Chelicerata (Chen et al., 1995b; Wills,1995; Legg et al., 2012, 2013), had a nervous system

organized as in Mandibulata. The nervous system ofAlalcomenaeus is more similar to that in Chelicerata,although the anterior pair of limbs on its head regionresembles the second pair of appendages of the pecto�ral segment in Stomatopoda.

Despite all their peculiar characteristics, Ediacaranand Early Cambrian organisms cannot be considered“helpless monstra,” not even as variations of “archaicdiversity” but as a world of organisms adapted to par�ticular environment that essentially changed duringthe Cambrian: from seas with low oxygen content inthe bottom water layers to well aerated waters filteredby the pellet conveyor belt; from a cold to warm cli�mate; from almost virgin, favorable substrates toalmost motionless and weakly attached filter feeders tostrongly bioturbated sediment (substrate revolution);from several slow predators to a vast diversity of activebenthic and nektonic chasers. For instance, the Cam�brian “explosion” was followed by the “Great Ordovi�cian Revolution.” The world of Metazoan organismsrenewed four times in the geologically short interval of80 Myr from the mid�Ediacaran to the beginning ofthe Ordovician: Late Ediacaran, Early Cambrian,Middle� Late Cambrian, and Paleozoic (formed in theOrdovician) biotas differed from one another morethan the Paleozoic biota differed from the Meso�Cen�ozoic, which existed for approximately 250 Ma each.

CONCLUSIONS: THE LONG OVERTUREOF THE CAMBRIAN “EXPLOSION”

Many hypotheses about the origin of life on Earthare faulty in that the evolutionary events are not linkedto the actual environment and everything in these the�ories happens in a kind of void. Some publications onthe Cambrian period suggest that the skeleton ofEcdysozoa was formed in animals inhabiting the lit�toral, partly submerged in water, whereas coastal areaswere covered by sand because of the washout from theempty, forestless land. In fact, all of the first Ecdysozoaand other animals lived in a normal marine sublittoralenvironment (Burzin et al., 2001, text�figs. 10.3,10.4), and the mineral skeleton in different groups,even within the Ecdysozoa, formed independently, atdifferent time and in each group, completely reflectingthe chemical composition of oceanic water of the cur�rent epoch (Zhuravlev and Wood, 2008; Maloof et al.,2010a; Kouchinsky et al., 2012). The expansion ofanimals first to the littoral and then onto the landbegan from the sublittoral (Mangano et al., 2014).Thick, sandy series began accumulating by the end ofthe Devonian Period with the appearance of forestsand mycorrhiza, a very strong destructive factor forrocks (Bonneville et al., 2009; Davies and Gibling,2010).

To some extent, with little connection to actualtime and space, Nielsen (2012, 2013, p. 171), pro�posed a hypothesis of primary ciliated holopelagicorganisms rooted in Haeckel’s “Gastrae” theory, say�



ing that “Information from the fossil record …andfrom genetics gives no direct information about theancestral eumetazoan life cycle.” According to this“superimposition model,” the holopelagic gastraeawas the ancestor of the eumetazoans with the indepen�dent addition of benthic adult stages in various clades.The opposing intercalation theory proposes a benthicgastraea with planktotrophic larvae evolving indepen�dently in numerous lineages through ontogeneticintercalations.

Nielsen based his theory on a comparative analysisof the embryology and morphology of extant represen�tatives of various phyla of Eumetazoa (Cretaceousechinoids, which he used as an illustration, is also amodern group, unrelated to the primary evolution ofEumetazoa and even echinoderms) and from theassumption that the independent, numerous appear�ances of a planktotrophic larva could not be adapta�tion�based. It appears that this assumption is not cor�rect, because the ancient organisms are far from beingidentical to their extant relatives morphologically andin lifestyle, and probably in embryogenesis. Forinstance, the protoconch in Cambrian mollusks andsome other Lophotrochozoa was larger than in latertaxa with a planktotrophic larva and thus indicatestheir benthic affinity (Nützel et al., 2007; Runnegar,2007). Brachiopods with a larval shell, which could beplanktonic, appear in the middle and at the end of theCambrian (Popov et al., 2012).

Thus, the fossil record presents several indepen�dent lines of evidence of planktotrophic larva being alate acquisition in Metazoans, even in the presence ofmany fossil embryos with direct development in theabsence both planktotrophic and lecitotrophic larvae(Donoghue et al., 2006). Direct evolution is observednot only in embryos of Cambrian Ecdysozoa but alsoin synchronous embryos of cnidarians and cteno�phores (Kouchinsky et al., 1999; Dong et al., 2013).

In addition, the planktonic and nektonic commu�nities with many metazoan animals were formed onlyin the late Cambrian–Ordovician, which is supportedby the morphological analysis of the body plan ofactual groups, and such important and independentpieces of evidence indicate the time of the beginningof the fecal pellet production, i.e., the time of the for�mation of the planktonic community (Signor and Ver�meij, 1994; Logan et al., 1995; Rigby and Milsom,2000; Butterfeld, 2001; Zhuravlev, 2001b; Vannier etal., 2007; Ponomarenko, 2008). On the whole, of the4367 genera of Cambrian fossils, 77% are motionlessbenthos (mollusks—308; halkieriids and others,primitive motile Lophotrochozoa—180; trilobites—2408; bradodoriidae and phosphatocopids—168;arthropods with nonpmineralized skeleton—118;ctenophores, cephalorhynchs and annelids, xenu�sians, anomalocaridids, parapsonemids remichor�dates and chordates—102; conodontophorides andchaetognaths 3) and 23% are attached or slightly mov�ing benthos (archaeocyaths and radiocyaths—309,

cribriciates—30; corallomorphs—32; stenothe�coids—16; brachiopods—233; hypoliths—78; orth�thecans—77; sabeliditids–lyditids—6; hyolithelm�inthes, tommotiids, and other primitive sessileLophotrochozoa—105; echinoderms—76, grapto�lites and pterobranchs—48) (Zhuravlev, 2001). If theevents are considered stage by stage, the proportion ofsessile and slightly moving taxa was approximately50% in the first half of the Cambrian, and by the mid�dle of this period it had decreased to 20%, whereas theproportion of the motile nektonic forms in the sameinterval increased from 5 to 20% (Wood and Zhurav�lev, 2012). Similar figures were obtained by compara�tive analysis of bio�volumes of the Early and MiddleCambrian communities: the number of individuals ofspecies (both planktonic and nektonic lifestyles)(Conway Morris, 1986; Ivantsov et al., 2005; Caronand Jackson, 2006; Dornbos and Chen, 2008; Zhaoet al., 2013).

Second, the Early Cambrian epoch shows anunusual high provincialism of marine fauns, which didnot have any equivalents in the whole of the Phanero�zoic history of Earth, even at the times of the largestregressions leading to the development of numerousisolated basins. The indicators of β diversity (the dif�ference of the specific and generic composition of theadjacent paleocommunities) reached the same valuesas the indicators of the γ diversity (the difference in thegeneric composition between the adjacent paleoprov�inces; the species composition was not entirely thesame (Zhuravlev and Naimark, 2005)). The same wasobserved in the Ediacaran period, although it isdescribed today only at the qualitative level, i.e., thereis a strict connection of certain paleocommunities toregional facies complexes (Grazhdankin, 2004;Lafamme et al., 2013). An exceptionally high level ofprovincialism is also observed among ichnofossils,although nothing seemingly should have obstructedthe parallel development of similar behavior forms indifferent groups, as in all later epochs (Jensen et al.,2013). This situation was unlikely to be possible, if theEarly Cambrian organisms had a planktonic stage intheir ontogeny.

As for the reasons leading to the appearance ofa planktotrophic larva, the most important was thesubstrate revolution, the development of which we canobserve from ichnofossils, a separate group of paleon�tological objects. In many cases traces are difficult tolink to organisms, but their examination facilitates anunderstanding of general trends in the evolution ofbehavior and in some cases point to the first appear�ance of some groups. It was previously thought that thefirst bilaterally symmetrical traces certainly indicatedthe presence of Bilateria. However, such tracks can bealso left by marine protists, like Rhizaria (Matz et al.,2008). In any event, tracks that can be linked to anyactivities of Bilateria, e.g., simple sinusoidal Helm�inthoidichnites, appeared only by the end of the Edi�acaran, later than vendobionts. An explosive diversifi�

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cation of traces of Bilateria began in the Cambrian,parallel to the diversification of skeletal organisms,and resulted in the formation of a well�developed,multitiered, and diverse infaunal community(Fedonkin, 1985; Droser and Li, 2001; Crimes, 2001;Gámez Vintaned and Liñán, 2007). All of these eventshappened in a normal marine sublittoral zone, fromwhich bioturbators had spread to the shallow water upto the periodically exposed littoral and toward thecontinental slope only by the mid�Cambrian. A sud�den increase in the rate and level of bioturbation, i.e.,by six times by the end of the Cambrian, resulted in aprofound impoverishment of the fauna of sessile andsedentary organisms; some of each, e.g., cnidarians,managed to colonize the pelagial (Wood and Zhurav�lev, 2012; Mangano and Buatou, 2014). This process isreferred to as the substrate or agronomic revolution(Seilacher and Pfüger, 1994; Bottjer et al., 2000). Theintensive, constant reworking of the substrate pre�cluded larvae from surviving on the surface of the sub�strate, whereas new communities in which the larvaecould attach and survive, e.g., hardgrounds and rock�grounds, had not yet formed (Vermeij, 1990; Zhurav�lev and Wood, 2008).

The effect of transcription factors and the expres�sion of various complexes of regulatory genes in thelarval evolution of mollusks, echinoderms, and someother groups indicate the independent and repeatedemergence of a planktotrophic larva and its mostimportant organs (apical plate, prototrach/neotrochs)in different groups of Bilateria (Sly et al., 2003; Dunnet al., 2007; Raff, 2008; Nakano et al., 2013). Evenvery similar larvae of chordates and Ambulacraliaappeared independently, based on the sequence ofgene expression (Lacalli, 2005; Swalla and Smith,2008).

In contrast, the total data on comparative mor�phology and embryology and molecular phylogeneticanalysis, including a comparison of the completegenomes and sequence of expression of the genes ofthe Hox complex, suggests that the stem group forBilateria were not just bilaterally symmetrical animalsbut triblastic animals (with muscle cells of mesoder�mal origin), apparently serial, with a distinct antero�posterior and dorso�ventral polarity and with an accu�mulation of nervous cells in the head region (Bala�voine and Adoutte, 2003; Prud’homme et al., 2003;Malakhov, 2004, 2010; Finnerty et al., 2004; Boeroet al., 2007; Gabriel and Goldstein, 2007; Arendtet al., 2008; Prpic, 2008; Williams et al., 2012; Chese�bro et al., 2013; Janssen and Budd, 2013). Forinstance, ctenophores have several types of mesoder�mal cells (muscular, mesenchymal, and others) andbranched off the rest of Metazoa before branching ofCnidaria and Bilateria. Assuming that the mesodermof Ctenophora is indeed homologous to that of Bilate�ria, the early development of the mesoderm in meta�zoan animals, with its subsequent loss in Cnidaria,Placozoa and possibly Porifera (Martindale and

Hejnol, 2009), and the genes necessary for that, areretained in sponges (Conaco et al., 2012; Kerner et al.,2013), given the resemblance of the expression of thecomplex of regulatory genes connected with the for�mation of the blastopore, mouth and anal openings inEcdysozoa (priapulids, some arthropods), Lophotro�chozoa (some mollusks, annelids, and nemerteans),and Deuterostomia, the structure of which is deter�mined by the original body plan for all Bilateria (Mar�tin�Duran et al., 2012). Moreover, ancestors of Bilate�ria, probably had serial paired appendages (Pangani�ban et al., 1997; Shubin et al., 1997; Jacobs et al.,2007; Prpic, 2008) that were most likely similar to cni�darian tentacles or the smooth appendages of somexenusians.

Indeed, the remains of sessile skeletal Lophotro�chozoa, which could be ancestors of brachiopods andother tentacle animals (tommotiids), appear in thefossil record later than remains of motile Lophotro�chozoa (mollusks and halkieriids) (Zhuravlev andWood, 2008; Maloof et al., 2010a; Kouchinsky et al.,2012). Even modern brachiopods retain some charac�ters of metamery, i.e., three body segments (Malakhovand Kuzmina, 2006), like phoronids, in which twosuch segments can be recognized (Temereva andMalakhov, 2006). Among Ecdysozoa, the oldestknown group is Xenusia with serial appendages, whichhave the original body plan in cephalorhynchs, on onehand, and in tardigrades, onychophorans, and arthro�pods, on the other (Gamez Vintaned et al., 2011;Caron et al., 2013b). The fossil record of chordate andechinoderms begins with bilaterally symmetricalorganisms, which have serial organization of someorgans, e.g., the gill apparatus (Shu et al., 2003b;Zamora et al., 2013).

Taking into account the data on the evolution of thecomplex of regulatory genes (Schierwater andDeSalle, 2001), germline cells (Buss, 1987; Black�stone and Jasker, 2003; Extavour, 2007), and larvaldevelopment (Blackstone, 2009), we can suggest theindependent evolution of bilaterally symmetrical andother multicellular animals, which was accompaniedby the parallel development of a number of structuresin both groups. These factors apparently explain theiralmost simultaneous appearance in the fossil recordand the parallel explosive diversification of sponges,cnidarians, ctenophores, and Bilateria as skeletal andsoft�bodied, as well as traces.

Could the Cambrian “explosion” truly happen, orit is only an epiphenomenon predetermined bychanges in the sedimentary settings at the Crypto�zoic–Phanerozoic boundary? The “explosion,” asmentioned above was not instantaneous; it was longerthan seconds or even a few million years. From theappearance of the first skeletal Metazoa (Namaca�lathus) and those possibly belonging to Bilateria 555 Mato the formation of the entire Metazoan assemblage(even if we do not omit bryozoans and groups absent inthe fossil record (echinoderms were the last to appear



as skeletons, ca. 515 Ma)), the duration of that calcu�lated explosion is 40 Ma, which is quite a long time.However simple the Ediacaran and Early CambrianMetazoa might have looked, these were relatively well�developed animals with a complete genetic apparatus,the assemblage of which needed a long time. If we can�not find clear precursors of these organisms, perhapsthe genetic apparatus could have evolved separatelyfrom them?

Indeed, the complex of the key Metazoan partici�pating in the embryogenesis, sexual reproduction, andapoptosis, i.e., the controlling factors regulating tran�scription (Brachyury, RUNX), adhesion, and polar�ization of cells in tissues (genes synthesizing catenines,laminines, cadherines and integrines), communica�tive intercellular systems (ancestral Notch�transcip�tion complex), cell differentiation (genes synthesizingtyrosinases), and genes producing neuromediators(neuropeptides) present in Choanofagellata, Ichthy�osporea (Creolimax, Sphaeroforma), Filasterea (Cap�saspora, Ministeria), Chytridiomycota, the basal groupof fungi, and Apusozoa (Amastigomas), and in fungiand choanoflagellates, part of this gene complex (from30 to 50%) could have been secondarily lost (Nicholset al., 2010; Sebe�Pedros et al., 2010; Fairclough et al.,2013; Suga et al., 2013; Suga and Ruiz�Trillo, 2013)(Fig. 1). This gene complex is turned on the stage ofthe formation of colonies and controls the synchroni�zation of cell division, and it is also used in the mitosisand production of protein necessary for building atubulin cytoskeleton, which is facilitated by alternativesplicing and enables the synthesis of different proteinson the basis of the same gene, which determines thegrowth of protein diversity and expands the complex�ity of gene regulation (Sebé�Pedrós et al., 2013).Except for Apusozoa, all of these organisms belong tosingle�celled organisms capable of forming colonies ofOpisthokonta, which are basal for the Metazoa(Chytridiomycota), whereas Apusozoa is probably asister�group of Opisthokonta and is the transitionalgroup between these organisms and Amoebozoa.

The latter group, based on the molecular data andstructure of organelles, is considered the sister groupof Opisthokonta, and both are assigned to Unikonta(Baldauf, 2008; Eme et al., 2011; Torruella et al.,2012).

The gene complex of Metazoa apparently beganforming before the appearance of Opisthokonta: inDictyostelia (previously assigned to the class Acrasio�mycetes in the section Myxomycota), the best studiedgroup of Amoebozoa, shows diverse signal Metazoanmolecules, including transductors, attractors, andactivators, causing aggregation and differentiation ofthe cell, which could include up to five different types(Saran et al., 2002; Eichinger et al., 2005; Schaap,2007), homeobox genes (Wariai), which are responsi�ble for the development of the antero�posterior axis(Han and Firtel, 1998), and proteins relative to α� andβ�catenins that playing a leading role in the adhesion

and polarization of epithelial cells, the synthesis ofwhich is increased during the formation of fruitingbodies, resulting in the formation of a polarized epi�thelium in Dictyostelia (Dickinson et al., 2011). It isimportant that slime molds have migrating pseudo�plasmodia, or aggregates of amoeboid cells, and cancross soil barriers impermeable for solitary cells(Kuzdal�Fick et al., 2007). This is an adequate reasonfor the evolution toward multicellurity. Thus, aggrega�tional, multicellular organization occurs among thelower Opisthokonta: amoeba Capsaspora, assigned toFilasterea, sister group, of Choanofagellata + Meta�zoa, and cellular slime mold Fonticula from Nuclear�iidae, sister group of Fungi (Brown et al., 2009; Sebé�Pedrós et al., 2013).

The eukaryote fossil record, which does not takeinto consideration various “plant” remains (Virid�iplantae, Stramenopiles), contains traces in the beds1.70–0.55 Ga similar to Horodyskia (they were origi�nally identified as hydroid colonies connected bythalli) (Fedonkin and Yochelson, 2002)], Myxomi�todes, and Gaojiashania (Fig. 1, Amoebozoa). Theydiffer from traces of bilaterally symmetrical animals inseveral characteristics: they are chaotic (traces of Bila�teria have a regular pattern; Fedonkin, 1985), formloops, bifurcate, vary in width within the same trace,and can become chains of globular structure (Bengt�son et al., 2007; Zhuravlev et al., 2009; Gámez Vin�taned and Zhuravlev, 2013). The mineralogical andelementary composition of the globular structure andtraces are also identical (Meyer et al., 2012). Suchtraces are in laboratory experiments are left by migrat�ing pseudoplasmodia Dictyostelia, which at the end ofthe life cycle form fruiting bodies as a globular head ofspores covered by a hard cover and attached by a stalk(Wallraff, E. and Wallraff, H.G., 1997; Sternfeld andO’Mara, 2005; Bonner, 2006). Another branch ofAmoebozoa (Lobozoa) exists at least 0.8–0.7 Ga andis represented in the fossil record by the shells Melano�cyrillium and similar forms (Porter, 2006).

Fungi that can be recognized from hyphae with orwithout septa, or by the presence on the same substrateof organisms characteristic for the lifecycle of fungi,are known from approximately 1.0 Ga in the fossilrecord (Burzin, 1993; Javaux and Marshal, 2006; Por�ter, 2006; Nagovitsyn, 2008; Butterfeld, 2009; Ger�man and Podkovyrov, 2010) (Fig. 1). The formerbelong to Ascomycota and the second belong to theChytridiomycota, although it is difficult to assign themto extant groups.

The first vendobionts appeared 0.58 Ga, represent�ing a transitional stage between the multicellular fungiand animals belonging to Opisthokonta: a rigid con�struction with a fractal system of canals suitable forosmotrophy above the substrate surface and inside thesubstrate (Fig. 1, Vendobionta). Apparently, by the endof the Ediacaran (not later than 0.55 Ga), the Meta�zoan gene complex in the ancestors of multicellularanimals had been completely formed, which predeter�

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mined the Cambrian diversification. Therefore, we seehere the almost synchronous appearance of primitivemembers of Ecdysozoa (xenusians, anomalocaridids,early cephalorhynchs and arthropods, later tardi�grades, pycnogonids, and pentastomids), Lophotro�chozoa (tommotiids, halkieriids and other celoscleri�tophores, hyoliths, stenothecoids, siphonocochs,ancient mollusks, brachiopods, annelids, and possiblykamptozoans, and later—bryozoans), Deuterostomia(early groups of echinoderms, hemichordates, andchordates), Ctenophora, Calcarea and Silicea(archaeocyaths, heteractinids, and others), Cnidaria(corallomorphes, hexaconylariids, hyolithelminthes,and later—conulariids and medusoids), and Chaetog�natha (protoconodonts), as well as an explosive growthof their diversity (Fig. 1).

This sequence of events does not agree well withmolecular clock data. However, the precision of themolecular clock is strongly influenced by unequal evo�lutionary rates within different groups, the selectedstatistical methods for primary data processing, andmany other assumptions of molecular biology, as wellas system biases (Ayala et al., 1998; Bromham, 2003).Therefore, drastically different molecular histories ofthe Bilateria exist—from long and cryptic ones thatare not reflected in the fossil record to those that areclose enough to an observed sequence of the firstappearances of diverse groups of organisms in the fos�sil record advocated above (Aris�Brosou, Yang, 2003;Peterson et al., 2004; Cartwright, Collins, 2007;Chernikova et al., 2011; Rota�Stabelli et al., 2013).

A compromise between the fossil record anda sequence of events suggested with the point ofa pipette is commonly searched for in those hypothet�ical ancestors of the Metazoa that could not be fossil�ized, e.g., Haeckel’s Gastraea.

A Gastraea�like metazoan progenitor would beimprobable, since the planktotrophic larva was a latedevelopment in the Metazoa, large planktonic andnektonic organisms did not exist at the beginning ofthe Cambrian, and all Cambrian fossil embryosbelonged to direct developers.

More attractive is Zakhvatkin’s (1949) hypothesisof a synzoospore, which was developed recently byMikhailov et al. (2009, p. 764). It suggests that a mul�ticellular animal appeared as the result of “…the evo�lutionary transition from temporal cell differentiationto spatial cell differentiation,” i.e., by the integrationof several cell types existing at different successiveancestor’s life cycle stages into a single multicellularfilter�feeding organism, which gave birth to all theother Metazoa.

However, in some specialized planktonic filterfeeders, e.g., Choanoflagellata, which are proposed asa hypothetical metazoan progenitor, a number ofimportant gene complexes have been apparently lost,whereas colony formation is carried out through celldivisions that are not synchronized, and sponge cho�anocytes arise from noncollared cells during embryo�

genesis and therefore are not homologous to choano�cytes in Choanoflagellata (Maldonado, 2004; Carret al., 2008; Fairclough et al., 2010, 2013; Sebé�Pedréset al., 2010; Suga et al., 2013).

Thus, the hypothesis of a planktonic filter–feedingancestry needs to be refuted and a different scenarioput forward, i.e., on the surface of the substrate inhab�ited by slime molds. Traces of organisms similar toslime molds are found on substrate surfaces dated1.70–0.55 Ga. Moreover, the only distinct evidence ofthe presence of the Metazoa and even the Bilateria inthe Pre�Cambrian, at the very end of the Ediacaran(<0.55 Ga), are marine trace fossils, including hori�zontal tunnels, surface tracks/trails, and vertical traces(Gámez Vintaned andLiñán, 2007; Chen et al., 2013).The surface tracks are particularly interesting, becausethe two series of parallel pits or scratch marks have abedding surface undisturbed between them (no trailleft by a body in between), indicating that they wereprobably left by an organism with appendages. To“make” a multicellular organism out of a conventionalslime mode organism (an amoeboid aggregate capableof movement), it is sufficient for the mechanisms thatturn on at the stage of the fruiting body formation (celldifferentiation, the epithelium formation, and thegamete germination) to became operational at thestage of the feeding motile stage of a slime mold withgametes. Such a confluence of two life stages wouldsimultaneously provide an opportunity for metazoangenes to be coopted from the genes and to be based ona regulating mechanism that previously functioned incell aggregations. In the unicellular Opisthokonta andDictyostelia, such regulatory mechanisms begin oper�ating during colony formation. The extant basalOpisthokonta are characterized mostly by clonal andsyncytial colonies, but the genetic toolkit responsiblefor cell adhesion and polarization and a cascade ofgene modifications, followed by multicellularity, isdeployed in aggregative amoeboid colonies (Sebé�Pedrés et al., 2013).

It is noteworthy that the Vendobionta show evi�dence of a life cycle similar to that of slime molds. Ven�dobiont fossils from the Trepassy Formation of south�eastern Newfoundland can be arranged in a successionof organisms (possibly a life cycle) consisting of organ�isms different in size and lifestyle but possessing thesame type of frondlets. The succession includes a fusi�form free�lying or even slightly motile Fractofusus—asedentary bush�like frondose Bradgatia—and a smallsedentary stalked frondose Charnia masoni growinginto a big one (up to 1 m high) Charnia grandis with awell�developed attachment disc (Brasier and Antc�liffe, 2004) (Fig. 1, Vendobionta). These could indeedrepresent an extinct intermediate group of the multi�cellular Opisthokonta, being neither fungus nor meta�zoan. Assuming that Metazoa are possible descen�dants of organisms resembling migrating slime molds,the Fungi could be descendants of its fruiting stage.



After all, we are all Unikonta and need to have a com�mon ancestor.

ACKNOWLEDGEMENTS

I am extremely grateful to the reviewers for theircritical review of the paper and for their useful com�ments and to the artist Vsevolod Abramov for makingreconstructions based on the author’s ideas. This workis supported by my own enthusiasm and the compas�sionate attitude of “National Geographic Russia.”

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Translated by S. Nikolaeva

the early history of the metazoa—a paleontologist’s … brachiopods are not intermediate between...

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