ISSN 20790864, 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.

The Early History of the Metazoa—a Paleontologist’s Viewpoint A. Yu. Zhuravlev Geological Institute, Russian Academy of Sciences, per. Pyzhevsky 7, Moscow, 7119017 Russia email: [email protected] Received January 21, 2014

Abstract—Successful molecular biology, which led to the revision of fundamental views on the relationships and 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 provides evidence for the hypotheses of molecular biology. The fossil record suggests that the different “phyla” now united 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 morphology of 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 biological disciplines, gives insight into their early evolutionary history, suggesting the existence of motile bilaterally symmetrical forms at the dawn of chordates, hemichordates, and echinoderms. Interpretation of the early history 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 relatives among the various earliest lophotrochozoans, some of which were sedentary suspensionfeeders while others were mobile epibenthic detritophages. In the aggregate, modern data from molecular biology, palaeontology, and comparative embryology/morphology, having been revitalized by the introduction of new microscopy techniques, imply that the hypothesized planktotrophic gastraelike common ancestor is the least likely of the diverse suggestions on the origins of the Metazoa. The common ancestor of the Bilateria had to be a motile epibenthic 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) period of the assembly of the metazoan genome within the unicellular and colonial common ancestors of the Opisthokonta, and possibly even the entire Unikonta. DOI: 10.1134/S2079086415050084

INTRODUCTION representatives of separate, long extinct phyla. Gould (1989), best known for the theory of “punctuated When Charles Doolittle Walcott discovered the first equilibrium,” was particularly supportive of this Lagerstätte (from the German Lager “storage,” approach, which suggested that fossils like Opabinia Stätte “place”) 100 years ago—the Burgess Shale in with five faceted eyes, lobes (flaps), and a segmented western Canada—everything seemed relatively sim proboscis or Hallucigenia with paired spines instead of ple: wormlike organisms were interpreted as annelid limbs and flexible unpaired limbs along the back, are worms, organisms with segmented limbs as arthro in fact artefacts of ancient Metazoa: they are not stem pods, and rounded imprints with radial lobes were groups to extant phyla, but taxa that competed with interpreted as jellyfish (Walcott, 1911a, 1911b, 1912). them for resources in the Early Paleozoic and ulti At the end of the 1970s, old collections from the Bur mately lost. gess Shale were reexamined, more samples were col At the same time, molecular biologists, based on lected, and new Lagerstätten were discovered. These comparative analysis of homologous DNA nucleotide include Chengjiang in South China, Sirius Passet For sequences and a comparison of the order of expression mation, northern Greenland, Sinsk Lagerstätten in of homeobox complexes, and later the comparison of Central Yakutia, Emu Bay Shale in South Australia, complete genomes, began to challenge the postulates and the Middle Cambrian Lagerstätten of Murero, of classical comparative anatomy. Their studies have Aragón in northeastern Spain, which yielded many of shown that arthropods are not related to annelids but, the most interesting fossils. At the same time it has together with priapulids and nematodes, form the become clear that the most interesting specimens did clade Ecdysozoa (periodically molting animals); not fit into the classical concepts of the comparative whereas brachiopods are not intermediate between the anatomy of the ancestral bauplan. These have been protostome and deuterostome animals but, together recognized, sometimes based on a few specimens, as with annelids, mollusks, bryozoans and other tenta

415 416 ZHURAVLEV cled animals, form another big clade, Lophotro timentifera, and also Rhombozoa) and Platyzoa chozoa (Halanych et al., 1995; Aguinaldo et al., 1997; (other Platyhelminthes, Gastrotricha, Acanthoceph Aleshin et al., 1998). Only Deuterostomia have ala, Micrognathozoa, and Rotifera); Lophotrochozoa remained as an unshakable bastion of comparative and Platyzoa are sometimes assigned together to Spi anatomy, although it included the enigmatic taxon ralia (Passamaneck and Halanych, 2006; Bleidorn Xenoturbella, once placed among flat worms. At first it et al., 2007; JiménezGuri et al., 2007; Sperling et al., seemed like a revolution that had failed to materialize, 2007; Dunn et al., 2008; Jenner and Littlewood, 2008; a game based on large numbers of unsubstantiated Marlétaz et al., 2008; Struck and Fisse, 2008; characters (Wägele and Misof, 2001; Nielsen, 2003; Yokobori et al., 2008; Egger et al., 2009; Struck et al., Philip et al., 2005). However, as time passed, these 2011 above papers). Based on purely molecular data, seemingly eccentric theories did not fade but instead the position of some organisms (Xenoturbella) and the became more clearly outlined (Baguñà et al., 2008; composition of some groups (Acoelomorpha, Colgan et al., 2008; Helmkampf et al., 2008; Hejnol Platyzoa) remain debatable: Xenoturbella, e.g., are et al., 2009; Paps et al., 2009; Braband et al., 2010; assigned together with Acoelomorpha to Deuterosto Ogino et al., 2010; Edgecombe et al., 2011; Telford mia (Philippe et al., 2011; Nakano et al., 2013) (Fig. 1). and Copley, 2011). Moreover, the ideas of molecular The relationships of some units within the Ecdysozoa, biologists were met with genuine interest and sup Lophotrochozoa and Deuterostomia, are still unre ported by the (literally) rockhard evidence provided solved. However, the multiplication of sequenced by paleontologists studying the morphology of Cam genes and species allows the determination in each of brian fossils. these groups of a suitable place for previous phyla that better agrees with concepts of comparative anatomy. Success in molecular biology outlined new param For example, data on 196 genes for 58 species of eters of phylogenetic trees and allowed the correct Lophotrochozoa revealed that Bryozoa, Phoronida, placement of the several problematic Cambrian and Brachiopoda are sister groups within the Lopho groups (e.g., Palaeoscolecida, Xenusia, Anomalocari phorata and established sistergroup relationships didae) among Ecdysozoa, as well as diverse Cambrian between Lophophorata and Kamptozoa+Cycliophora objects known as “small shelly fossils.” Only 10– (Nesnidal et al., 2013), whereas previous insufficient 15 years ago these 20–30 large groups (tommotiids, sampling had united brachiopods, phoronids, and halkieriids, Hadimopanella and many others), which nemerteans in the bizarre group Kryptrochozoa comprise a considerable proportion of Cambrian (Dunn et al., 2008; Giribet et al., 2009). diversity, appeared never to have been confidently placed anywhere in the phylogeny of Metazoa. The problem of the basal groups—sponges, cni darians, Trichoplax, and triploblastic ctenophores— The Metazoan molecular trees are presently subdi remains a tangled knot in the evolution of Metazoa. vided into the braches Porifera (Hyalospongia, Demo After the discovery of Homoscleromorpha were previ spongia and Calcarea, and also Homoscleromorpha), ously considered a family and suborder in the class Placozoa (Trichoplax), Cnidaria (including Myxo Demospongiae with a basal membrane consisting of zoa), Ctenophora, Acoelomorpha (nemertodermatids collagen IV and laminine underlining the choano and and Acoela, sometimes with Xenoturbella), Deuteros pinacoderm and ciliate epithelium in the cincto tomia (echinoderma, hemichordates and chordates, blastula. Homoscleromorpha and spermatozoids with sometimes together with Xenoturbella), Chaetog hacrosomes, i.e., characters unknown in other natha, Ecdysozoa (nematodes, Nematomorpha, Pri sponges but typical of triblastic Metazoa, were recog apulida, Loricifera, Kinorhyncha, Tardigrada, Ony nized as a separate class of sponges, and this assign chophora, Arthropoda, including Pentastomida), ment was supported by molecular data (Ereskovsky Lophotrochozoa (Bryozoa, Kamptozoa, Cyclio et al., 2009; Gazave et al., 2012). Working hypotheses phora, Orthonectida, Brachiopoda, Phoronida, Mol on the succession of appearances and relationships of lusca, Nemertea and Annelida, including Myzosto various sponges, cnidarians, ctenophores, and Tri mida, Echiurida, Sipunculida and Pogonophora / Ves 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 (Cambrian Ctenorhabdotus), 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 (Cambrian palaeoscolecid worm), Priapulida (Cambrian Yunnanpriapulus), Tommotiida (Cambrian Camenella), Vendobionta (lifecycle of the vendobiont Fractofusus + Charnia), Vetulicolia (Cambrian Vetulicola), Xenusia (Cambrian Microdictyon). © Artist Vsevolod Abramov.

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1700 1000580 550 540 million years Amoeboza Apusozoa Nucleariidae Fungi Vendobionta Ichthyosporea Filasterea Choanoflagellata Hexactinellida Demospongiae Calcarea Homoscleromorpha Ctenophora Placozoa Cnidaria Xenoturbellida Nemertodermatida Acoela Cephalochordata Urochordata Craniata Echinodermata Hemichordata Chaetognatha Tardigrada Anomalocaridida Onychophora Xenisia Arthropoda Vetulicolia Priapulida Loricifera Kinorhyncha Palaeoscolecida Nematoda Nematomorpha Mollusca Annelida Coeloscleritophora Nemertea Bryozoa Brachiopoda Amoebozoa Phoronida Cycliophora Kamptoza Gastrotricha Tommotiida Platyhelminthes Gnathostomulida Micrognathozoa Vendobionta Rotifera

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 418 ZHURAVLEV tory (Borchiellini et al., 2001; Malakhov, 2004, 2010; lacking protective organic films, and the mixing of sea Wallberg et al., 2004; Schierwater et al., 2009; Pick floor sediment matrix by bioturbators (borrowing ani et al., 2010; Ryan et al., 2010; Martindale, 2013). mals), which results in situations in which a coquina Apparently, to catch the molecular signal of phyloge bed only 1 cm thick can contain fossils that have accu netic branches that diverged early in phylogeny, a sim mulated over 15000 years. The low oxygen level in the ple accumulation of molecular data is insufficient, Cambrian basins (Saltzman, 2005; Gill et al., 2011) even when all of these data are based on the analysis of was an important condition for the formation of orthologs. It is essential to analyze the groups of genes Lagerstätten, because it prevented activity of bioturba that most clearly show early branching in the evolution tors. In the absence of bioturbators, organisms were of basal Metazoa, e.g., ribosomal genes (Pick et al., preserved in their entirety, rather than as disassembled 2010; Philippe et al., 2011; Nosenko et al., 2013). In segments, spicules, or sclerites. In organisms with a rigid addition, it should be understood that all modern cuticle, the rate of mineralization of soft tissues (their groups in their evolutionary history passed through the replacement by clay minerals, silica, pyrite, or phos bottlenecks of mass extinctions, which could severely phate) could be greater than their decomposition rate. deplete their genetic diversity, e.g., as was observed in Therefore, the Cambrian Lagerstätten of the “Bur ctenophores (Podar et al., 2001). Since the addition to gess type” primarily contain mineralized casts of rela the molecular dataset of data from a single group of tively large animals with a developed cuticle. Of these, Monoplacophora changes the entire architectonics of cuticular remains of Ecdysozoa as isolated larval skins mollusk molecular trees (see below), it seems unlikely or, less commonly, casts of organisms with some min that molecular trees are sufficient on their own, with eralized soft tissues constitute 70% or more of the total out paleontological data, to resolve dozens of such key number of species and individual organisms in the fos groups. sil assemblage and of its total biovolume (in paleoecol ogy this parameter is used instead of the biomass) SEDIMENTOLOGY AND TAPHONOMY (Conway Morris, 1986; Ivantsov et al., 2005; Caron AS A BASIS FOR MODERN PALEONTOLOGY and Jackson, 2006; Dornbos and Chen, 2008; Zhao et al., 2013). The “taphonomic window” (the interval Before continuing with the next section, it is worth with the most Cambrian Lagerstätten) opened when bearing in mind that the end of the Cryptozoic–begin Ecdysozoa acquired rigid cuticles and closed when the ning of the Phanerozoic eons/eonothems of the Inter oxygen levels in relatively deep marine basins national Chronostratigraphic Scale is subdivided in to increased, facilitating bioturbators, which in turn the Cryogenic (850–635 Ma), Ediacaran (considered increased aeration of the sediment. The Cambrian to be equivalent to the Vendian in Russia) (635–541 Ma), Ecdysozoa include Arthropoda, Cephalorhyncha, and Cambrian (541–485 Ma), and Ordovician (485–443 Ma) exinct groups (classes or stem groups using cladistic periods/systems (radiometric data of the absolute age terminology), i.e., Xenusia (with a wormlike annu are in brackets). The Cambrian period/system until lated body, lobopodian retractile legs, and a long pro recently included three epochs/series: Early/Lower boscis), Anomalocarididae (with compound stalked (541–509 Ma), Middle/Middle (509–495 Ma) and eyes, segmented grasping appendages in front of the Late/Upper (495–485 Ma); this division is accepted mouth, triradiate oral cone possessing plates, and here for simplicity. A distinct boundary between the swimming lobes) and, perhaps, Vetulicolia (Hou and eonothems, noted in the 19th century and drawn at Bergstrom, 1995; Budd, 1998; Hou et al., 2006; Ma the base of the Cambrian system, is related to the mass et al., 2009; Harvey et al., 2010; Gámez Vintaned appearance of organisms with a mineral skeleton, et al., 2011; Zhuravlev et al., 2011b) (Fig. 2). Cha leading to the subsequent formation of localities with etognatha, Hemichordata, and Chordata with a rela abundant burials of “softbodied” animals. tively thick epithelium (Shu et al., 2003b; Chen and The “softbodied” organisms are preserved in par Huang, 2002; Caron et al., 2013a), Cnidaria with chi ticularly strictly defined environments which are tinized tubes, and Ctenophora (Conway Morris and referred to as Lagerstätten. The Cambrian Lagerstätten Collins, 1996; Hou et al., 1999) constitute another 5%. are thin (composed of claysize particles, ≤ 4 μm) sedi The remaining 25% are represented by sponges, echi mentary rocks usually of marine origin with limited noderms, mollusks, annelids, and the Lophotro oxygen content. Organisms were carried to these chozoa, the preservation of which in Lagerstätten dif places by turbidity currents, underwater mudslides, or fers from that in normal deposits only in that their other fast events (Ivantsov et al., 2005; Caron and skeletal elements, including nonmineralized ele Jackson, 2006; Gaines et al., 2012). The surface of ments, remain in a lifelike position. Brachiopods, beds with assemblages of such fossils organisms there mollusks and annelids rarely have primary chitinous fore represent instantaneous casts of ancient events chaetae, or during phosphatization, imprints of cells, (rather than an averaged representation, as occurs in even of microvilli on the shell surface (Ushatinskaya the deposits that are accumulated in normal condi and Parkhaev, 2005). In addition, in the remains of tions during the rapid processing of organic matter by brachiopods and other tentacled animals with strongly scavengers and decomposers), the dissolution of shells chitinized covers, it is sometimes possible to discern a

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j

h g

i

c

f d e

b 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 and Caron (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. pedicle, digestive tract, and lophophore with ciliated remains, including embryos, larvae, and fragments of tentacles (Zhang et al., 2004, 2009). It is possible to large organisms, all of which except in extremely rare estimate other ecological parameters, e.g., species instances, belong to Ecdysozoa (Müller, 1979; Maas et diversity or abundance, with the same total result: al., 2006). The phosphatized embryos, which should Ecdysozoa is the overall dominant group (Zhao et al., be arranged in successions from the initial stages of 2013). In other types of occurrences, molluskan “bod cleavage to gastrulation and the development of the ies” are preserved in extreme circumstances, e.g., in adult organism, are sometimes assigned to cteno the Silurian Herefordshire Lagerstät (425 Ma), where phores, cnidarians, and some inserta sedis groups, they were preserved as calcite infills within nodules such as Pseudooides, whereas Lophotrochozoa are entombed in an ancient volcanic ash (Sutton et al., absent (Bengtson and Yue, 1997; Kouchinsky et al., 2001, 2012). 1999; Chen et al., 2007), although the Ecdysozoa The Örstentype Lagerstätten, named after the affinity of some embryos of “Cnidaria” or “Cteno type Late Cambrian locality in Sweden, in contrast to phora” cannot be completely excluded (Liu et al., the Burgesstype, contain only small phosphatized 2014; Steiner et al., 2014).

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Orstentype Lagerstäten are mostly found in the Weng’an fossils showed that irregularly elliptical Ediacaran and Cambrian beds and were probably 32cell stage objects resemble embryos with a visible formed when anoxic water masses upwelled into the micromere cap at one end and macromeres arranged shallow shelf or resulted from intense hydrothermal in a row at the opposite end, nearer the “ventral side.” activity (Donoghue et al., 2006; Yin et al., 2014). The In gastrulae such a row precedes the development of bestknown Ediacaran Lagerstät of this type is a Dous the gust, whereas micromeres give rise to integument hantuo phosphorite Lagerstätte, in Guizhou, South cells (Chen et al., 2009; Yin et al., 2013, 2014). It must China, in the thick phosphotite Weng’an member be noted that, among the millions of phosphatized (630–620 Ma). This locality contains giant acritarchs, microfossils, multiple objects with similar shape or algae, presumed embryos, sponges, corals, and the complexity can be found, like finding a pebble strik earliest Bilateria (Vernanimalcula) with a circulatory ingly similar to a chicken bone on a large beach. Thus, system, paired coelomes, gut, etc. (Li et al., 1998; the Doushantuo phosporites suggest so far that multi Chen et al., 2004; Liu et al., 2008). Bengtson et al. cellular algae (Viridiplantae or Stramenopiles) existed (2012) published a particularly high impact paper on at the beginning of the Ediacaran period (which, in Vernanimalcula, in which they calculated that the fact, appeared earlier, see Butterfeld, 2009)—possibly original article by Chen et al. (2004a) has attracted even in simple embryos in the early stages of splitting. more than 160 citations, including publications on the As for the Cambrian Lagerstätten, it should be said origin of bilateral symmetry, the circulatory system, that the dominance of Ecdysozoa in all these assem eyes, and even cancer. However, the paper by Bengt blages is related not only to good preservation of their son et al. (2012), entitled (with reason) “A Merciful integuments but also to the geochemistry of the Edi Death for the ‘Earliest Bilaterian,’ Vernanimalcula” acaran–Cambrian oceans, which still retained fea concluded, based on the study of fibronormal crystals tures of the stratified Canfield Ocean (Canfield, 1998). of the apatite minerals forming this fossil, that all “lay The deep layers of this ocean were largely euxinic to ered tissues” and “organs” were the effects of mineral anoxic (which spread to shallow waters during regres ization of phosphatized layers formed at various stages sions), which was concluded based on sedimentologi of diagenetic (secondary abiogenic) modification of cal, mineralogical, and isotope analysis (34S/32S, organic matter of uncertain origin possessing micro 13C/12C) and the increased content of Mo, U, and V scopic cracks. The socalled spiculate sponges from (Li et al., 2010; Gill et al., 2011; Pi et al., 2013). Some the Weng’an phosphorite are likewise of inorganic Ecdysozoa are adapted to such conditions. Among nature: neither the microstructure, nor chemical com Loricifera, there are obligatory anaerobic taxa surviv position of micrometersized acicular structures pro ing anoxic conditions due to hydrogenosomelike vide substantial evidence for their assignment to organelles (Danovaro et al., 2010), while priapulids sponge spicules (Yin et al., 2001). The structures inter and nematodes can live through long periods of anoxia preted as “corals,” in light of their microscopic size (Oeschger, 1990; Vanreusel et al., 2010). Analysis of (diameter less than 100 μm), very regular dichotomous the deepest water Cambrian assemblages (sublittoral) branching and arrangement of tabulae, as well as the shows that they included species with different adap lack of partitions, are renalcids—organisms of uncer tations to life in an oxygendepleted environment tain affinity resembling some algae from the groups (Ivantsov et al., 2005). Viridiplantae and Rhizaria that were common in the This taphonomic background was necessary, EdiacaranCambrian (Liu et al., 2010; Zhuravlev because the appearance of the ancient organisms and et al., 2011a). their role in the paleocommunities are largely judged Phosphatized embryos were also difficult to inter from the analysis of Lagerstätten. Such an analysis is pret. The socalled embryos were spherical microfos impossible without a basic knowledge of sedimentol sils (on average 300–650 μm across) with a distinct ogy (study of the processes of formation of sedimen polygonal ornamentation composed of smaller tary deposits) and taphonomy (study of transforma spheres (Xiao et al., 1998). However, the same appear tion of dead organisms into fossils). These fields serve ance is observed in cysts of Holozoa (Protista) (Huldt as the basis for modern paleontology. From the view gren et al., 2011), Viridiplantae, and giant sulfur bac point of taphonomy, conclusions recently published in teria (Bailey et al., 2007), and even layers of diagenetic prestigious journals by Smith and Caron (2010) and phosphate mineral (Bengtson and Budd, 2004). Min Smith (2013), seem insufficiently substantiated. These eralogical study of these microfossils and their chemi publications address the occurrence in the Cambrian cal element composition (C, Ca, P, and F) showed that rocks of numerous samples with imprints of the soft the multiple layers cannot be interpreted as original bodied cephalopod Nectocaris pteryx (this organism cellular layers; they were mainly formed in late diagen was previously interpreted as belonging to Arthropoda esis, thereby excluding the possibility of interpreting or Chordata) (Fig. 2h). The probable existence of such these structures as colonial bacteria or embryos such as an ancient cephalopod, which, as reconstructed by gastrulae (Cunningham et al., 2012a, 2012b). Imaging Smith and Caron (2010) and Smith (2013), had paired techniques using propagation phasecontrast based cameralike eyes on short stalks, lateral fins, well synchrotron radiation microtomography of some developed gills, and a funnel (hyponome) suitable for

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 421 jet propulsion, revolutionized the interpretation of the THE TALE OF HOW MOLECULAR BIOLOGY early evolution of cephalopods. Until recently it was MET PALEONTOLOGY, believed, based on paleontological evidence, that the WITH CONSEQUENCES coleoid cephalopods in the Devonian Period (ca. 400 Ma) FOR COMPARATIVE ANATOMY had evolved from cephalopods with an external shell, which originated in the Cambrian from some kind of Trichoplax and the Vendobionts monoplacophorans or gastropods. These old recon The study of the complete mitochondrial genome structions need to be fundamentally critically revised. of Trichoplax showed that it contains regions unique to It is not surprising that malacologists were skeptical the Metazoa, and also includes introns similar to those about the above interpretation. They noted that the of chytrid fungi and Choanoflagellata; this genome is animal could not have had a gut if the axial cavity larger than the mitochondrial genome of any other clearly visible in the fossil imprints was a mantle cavity. Metazoa (43079 bp) due to large intragenic spacers However, if that was a gut, then the structures in it and genes encoding proteins of unknown function could not have been gills; the hyponome lacked a cir (Dellaporta et al., 2006). Although the complete cular mantle muscle and widened distally and thus was genome of this organism, which was later sequenced, unlikely to be suitable for jet propulsion; and there was was shown to be more complex than previously only one pair of frontal tentaclelike appendages thought, suggesting secondary loss and simplification (Kröger et al., 2011; Mazurek and Zaton, 2011; Run of the animal (Srivastava et al., 2008), Trichoplax was negar, 2011). The presence of one hundred mollusk accepted as an ideal model of the basal stem organism specimens (if Nectocaris is interpreted as a mollusk) for all metazoan animals (Rozhnov, 2010; Sperling lacking a shell is doubtful in itself. Smith (2013) indi and Vinther, 2010). The authors came to this conclu cated that the covers of this fossil, which were replaced sion after having studied Trichoplax and compared a by the clay mineral chlorite, has an elevated calcium series of its feeding traces with those of Vendobionta. concentration. Chlorite of such composition is formed However, it is unlikely that the mode of locomotion of when clay minerals replace originally strongly miner a millimetersize Trichoplax using flagellated cells of alized tissues of the calcareous skeleton (Zhuravlev et the ventral epithelium could be used by organisms that al., 2011b). In Smith’s opinion the gills in Nectocaris were larger by three orders of magnitude. could be phosphatized. However, the position of this Seilacher (1989, 1992) coined the name Vendo complex of organs along the axial cavity and their bionta for large (up to 1 m long or longer) Ediacaran prominence and phosphatic composition suggests that fossils composed of segmentlike units (frondlets), these were digestive diverticula (Butterfeld, 2002; which, unlike true segments, can be arranged along Zhang and Briggs, 2007; Zhuravlev et al., 2011b). any axis of an organism and form a relief quilted sur Conversely, gills in Cambrian argillaceous Lagerstät face (Figs 3a–3h). These fossils had previously been ten are not phosphatized, while phosphatized gills are placed within the jellyfish, mollusks, annelids, echin found in Mesozoic anoxic marine deposits, but in that oderms, etc., although they resemble these animals case other soft tissues are also phosphatized. Therefore only in artistic reconstructions (Glaessner, 1984; Jen the axial cavity of Nectocaris is interpreted as a straight kins, 1992; Dzik, 2011). Authors occasionally do not gut with a terminal anus and mouth at the end of the notice that the fossil animal assigned to Proarticulata “hyponome,” which is adjacent to the gut. In this case differs from a cast interpreted as a diploblastic animal the “hyponome” is a proboscis, the tentacles are only by a slightly less pronounced spiral arrangement paired mouthparts, and the coarse stripes along the of frondlets (e.g., Paravendia janae (Ivantsov, 2004) fins are external gill filaments. This complex of organs and Eoandromeda octobrachiata (Zhu et al., 2008)) is typical of anomalocaridids (Ecdysozoa) common in (Figs. 3g and 3h). the Cambrian Lagerstätten (Budd, 2001; Daley et al., According to radiometric dating, Vendobionta are 2009) (Figs. 2g and 2i). The presence of cameralike found in beds 579–543 Ma in age (Martin et al., 2000; eyes does not contradict this conclusion, as similar Lafamme et al., 2013). Fedonkin (1983, 1987) was the eyes are found in Ecdysozoa, e.g., in extant arthropods first to notice that many of these organisms have a sim (Land, 2005) and onychophorans (Mayer, 2006), and ilar type of segmentation and glide reflection symme also in Cambrian Xenusia (Schoenemann et al., try (expressed as a halfstep shift of the conditionally 2009), which are close relatives of anomalocaridids. left frondlets in relation to the mirrored right frondlets A detailed analysis of Smith’s work was necessary, along the body axis) that is not observed in any Meta because neonatologists sometimes too quickly accept zoa (Figs. 3b–3g). Such fossils are frequently inter the conclusions derived from such publications. If preted as ancient worms or arthropods. Apart from a these papers are published in highimpact journals, particular type of symmetry, the major groups of Ven they have every chance of a long life, and, as Bengtson dobionta (Triradialomorpha (Fig. 3a), Rangeomorpha et al. correctly pointed out, a fairly “merciful death” (Figs. 3b and 3c), Arboreomorpha (Fig. 3d), Petal may go unnoticed. This does not mean that paleonto onamae (Fig. 3e), Proarticulata (Figs. 3f and 3g), logical evidence cannot be trusted, but some interpre Bilateralomorpha) are similar to one another and dif tations of this evidence can be deeply erroneous. ferent from Metazoa in the absence of a mouth, anus,

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j

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d g

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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. gut, any kind of zooids and unlimited, not isometric, in the same beds (Grazhdankin and Seilacher, 2002; growth with terminal, including bipolar, asymmetric Grazhdankin, 2004; Zhu et al., 2008). insertion of new frondlets (Zhuravlev, 1993a; Grazh However, the largest difference is in the internal dankin and Seilacher, 2002; Peterson et al., 2003; Ant structure of the organisms, in the presence of a system cliffe and Brasier, 2008; Naimark and Ivantsov, 2009). of tubelike units chambers (vanes) that are subquad In addition, vendobionts are often preserved in large rate in a crosssection and penetrating the entire body numbers in coarsegrained sandstones, without losing (the length of the chambers greater than the width by one–two orders of magnitude) (Petalonamae (Fig. 3e), details of their morphology, which is impossible even Proarticulata (Fig. 3f), Bilateralomorpha) or thin for organisms with a mineral skeleton. The coarser the bifurcating canals arranged in one plane (Rangeomor sediment is, the more prominent is the morphology of pha (Figs. 3b, 3c, and 3j), Arboreomorpha (Fig. 3d)), vendobionts. When the same species are buried in a which was revealed using high resolution laser scan finegrained sediment, they have on their surface a ning and digital mapping. It is this system of units that rigid organic film present in the fungi and algae found gives vendobionts their quiltlike appearance (Xiao et

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Fig. 4. Cambrian (a–u) and Ordovician (e) Lophotrochozoa: (a, b) – “tommotiids” (a) Paterimitra, (b) Camenella (c, d) celo scleritesloclescleritophores: (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. al., 2005; Brasier and Antcliffe, 2008; Brasier et al., All of this suggests that vendobionts occupy a sepa 2012). Both systems are of the closed type, i.e., they do rate position among multicellular animals, i.e., that not communicate with the outside environment by they in fact are not connected with Metazoan evolu any kind of pores. The tubelike chambers contact one tion. The distribution of vendobionts in the aphotic another along their entire length (Grazhdankin and zone of the ocean or their existence under the surface Seilacher, 2002; Brasier and Antcliffe, 2008). The of the sediment excludes their possible algal sensu lato canals uniformly fill the entire body, including the affinity and the presence of photosymbionts (Grazh “head” in Proarticulata and Bilateralomorpha dankin, Seilacher, 2002; Peterson et al., 2003). Like (Ivantsov, 2004, textfigs. 4–6); as they approach the wise, they are not directly related to fungi or lichens, surface, the canals bifurcate from three to five times, with which they are sometimes compared (Retallack, progressively decreasing in diameter, resulting in a 1994; Peterson et al., 2003), because the continuous fractal pattern like Escher’s “Regular Division of the fractallike system of canals of various crosssections, Plane.” In some Proarticulata, e.g., Dickinsonia, the as well as the tubelike chambers characteristic of ven system of tubes is combined with canals (Ivantsov, dobionts, had nothing in common with the cylindrical 2004, pl. 1, fig. 7). hyphae of fungi, which at comparable length are sub

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 424 ZHURAVLEV divided by septa. This branching system of canals/ the environment. In the event of an exhausted chambers allowed vendobionts to absorb dissolved resource, e.g. precipitated organic suspension or bac organic matter forming compact multitiered bottom terial mat, such a signal would be also detected by a communities (the upper tier reaches 2 m) in environ vendobiont. ments with very slow currents (not more than 1–5 cm/s) The content of dissolved, colloidal, and suspended (Burzin et al., 1998; Sperling et al., 2007; Lafamme organic matter in the Ediacaran ocean was 2–3 times et al., 2013; Ghisalbert et al., 2014) (Figs. 3b and 3d). higher than the present level, which is determined by This system of canals, chambers and frondlets, which the proportion of the isotopes of Ca, N and organic enable the organism’s growth, allowed vendobionts to carbon (Fike et al., 2004; ShieldsZhou and Zhu, retain a body area to volume proportion of 1 × 1000 × 2013; Kikumoto et al., 2014). It is no coincidence that 102 mm–1, whereas this ratio in osmotic megabacteria other giant osmotrophs are characteristic of the Edi reaches 1 × 101 mm–1 or more, although their size does acaran: bacterial colonies and fungi (Marusin et al., not exceed 0.75 mm (Lafamme et al., 2009). Biome 2011). In the modern oceans, megabacteria, the largest chanical experiments with plastic models of lobelike osmotrophs, are concentrated in upwelling zones, i.e., stalked vendobionts in tanks showed that the “quilted” in conditions of a stable biogene flux (Schulz, H.N. and relief directed the water current along the body sur Schulz, H.D., 2005). The diversification of vendo face, whereas the resulting vibration of the lobe, bend bionts began in the zone of counter currents and ing parallel to the current, reduced the load of the cur upwelling of the subpolar sea (Fedonkin, 2000; rent and at the same time boosted the exchange of flu Lafamme et al., 2013) and continued in an environ ids with the environment by facilitating the diffusion ment of increased content of oceanic organic matter of dissolved matter. The current rate dropped due to with frequent drops in the oxygen level and the the relief of the lobe, while the mixing of the water absence of bioturbators and predators. A decrease in mass along the lobe increased (Singer et al., 2013). the significance of the first of these factors and a sharp Suspension feeding required a constant, relatively increase in the significance of the latter led to a com strong (over 5 cm/s) current, threedimensional filter plete disappearance of vendobionts at the Ediacaran– ing organs (flagellate chambers of sponges, lopho Cambrian boundary. The carbon isotope anomalies phore of brachiopods, gills and bivalve siphons), recorded for the deposits of this age suggest a large whereas the suspension feeder should be positioned turnover of the carbon cycle, which has no equivalent perpendicular to the current (Vogel, 1988) and not in the Earth’s subsequent history. Although the occur bent along it (like thalli of ribbonlike algae), as is sug rence of vendobionts from younger deposits are fre gested for vendobionts. quently mentioned (e.g., Conway Morris, 1993; Bab Vendobionts lying freely on the bottom and those cock and Ciampaglio, 2007), none of these records living in the subsurface growing through the substrate meet the above morphological criteria. They either or even through adjacent (already dead?) individuals represent the remains of normal Phanerozoic organ were also osmotrophs (Grazhdankin and Seailacher, isms, or fossil traces, or sometimes inorganic struc 2002; Droser et al., 2014), because they are organized tures. exactly like stalked taxa (Figs. 3a, 3c, and 3e–3i). The morphology of Ediacaran skeletal organisms is Traces of vendobionts are traces of absorption, engulf interesting. For instance, the most common of them, ing, and the showing of imprints of the branching Cloudina, has a very unusual skeleton consisting of canal system (Ivantsov, 2011, pl. 2, fig. 4). They could eccentric calcareous cones nested within one another only appear if the organism was very tightly sucking on and with closed bases; the microstructure of the skele the substrate by its entire surface. An unusual, discrete ton is primitive and is found in red and other calcare movement of vendobionts to a distance not greater ous algae (Viridiplantae), foraminifers (Rhizaria), than a third of their length (Ivantsov and Mala sponges and Cnidaria (lower Metazoa); in annelids, khovskaya, 2002; Ivantsov, 2011), as well as a slight including pogonophores, this microstructure is not reduction of the surface (Brasier and Antcliffe, 2008), found. No protoconch has been found in Cloudina, were apparently performed by the same systems of but a basal opening is present (Cortijo et al., 2010; canals. A change in osmotic pressure would allow the Vinn and Zaton, 2012; Zhuravlev et al., 2012). Nama surface area to be decreased and remove the organism calathus has a calcareous skeleton in the shape of a from the substrate. For further movement at the sur porous polyhedron on a stalk. No stolon or polypoid face to volume ratio, even a small current or low waves characters are observed (Grotzinger et al., 2000). would be sufficient. A similar mechanism is presently Namapoikia is a shapeless honeycomb mass. Suvorov used by predatory fungi, which are able (in 0.1 s) to ella and Majaella are possible skeletal vendobionts, absorb more water into the cells and increase their vol Sinotubulites is a cylindrical shell of irregular layers of ume, catching and immobilizing a round worm or a aragonite. Anabarites is spirally coiled conical shells water bear, by changing the osmotic pressure in the with three lobes (Vologdin and Maslov, 1960; Kouchin hyphae quickly (Heintz and Pramer, 1972; Chen et al., sky and Bengtson, 2002; Wood et al., 2002; Chen 2001). The fungal activity is initiated by a change in et al., 2008; Zhuravlev et al., 2012). All of these earli the concentration of different elements (e.g., C/N) in est skeletal organisms disappeared at the end of the

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Ediacaran–beginning of the Cambrian period and, in extinct within the Early Cambrian, with only two spe light their unusual morphology, have nothing in com cies known from the Middle and Late Cambrian beds. mon even with the subsequent Cambrian “explosion.” Since both were suspension feeders, the assignment of Namacalathus (see below). archaeocyaths to sponges is supported by biomechan ical studies of skeleton models, usually a porous cup with vertical and/or horizontal porous septa connect Sponges: Not Spicules Only ing walls in tanks (Savarese, 1992), and the analysis of Sponges are widely believed to be the first Metazoa trends in evolutionary changes in their skeletal ele in the fossil record, although all early occurrences of ments toward improving filtration (Zhuravlev, 1993b). these organisms are debatable. Biomarkers (indestruc Judging from the skeletal microstructure, body plan, tible remains of some aromatic and aliphatic hydro and the nature of asexual reproduction and immune carbons (Peters and Moldowan, 1993; Summons reactions (fossil reefs retain skeletons in lifelike posi et al., 2006)), i.e., 24isopropylcholestanes, specific tions and in relationships with related and unrelated for this group and abundant in the Ediacaran oilbear organisms), archaeocyaths were most similar to mod ing and carbonate deposits, suggest that sponges could ern sponges, which include taxa with calcareous skel have existed 635 Ma (Love et al., 2009). However, etons with no spicules, similar to the skeleton of Love et al. do not exclude the possibility that these are archaeocyaths, Acanthochaetetes, and Vaceletia molecular remains “of their ancestors” (Love et al., (Zhuravlev, 1989; Debrenne and Zhuravlev, 1994) 2009, p. 719). It is quite possible that these biomarkers (Fig. 1). Hemispherical radiocyaths were the largest belong to algae (Stramenopiles) and are diagenetically abundant, though not diverse, Cambrian reef builders altered (Antcliffe, 2013). Reitner and Wörheide of supposedly sponge affinity. Their skeleton was com (2002) recorded spicules in the cryogenic dolomite posed of dumbbelllike elements with stellate plates on Noonday (750 Ma) in Nevada; illustrations of the spi the ends, which, by contact with rays, formed porous cules have not been published, but this paper is often outer and inner walls. Their only equivalents and cited as a primary source (Müller et al., 2007; Sperling probable descendants were Ordovician–Permian et al., 2010). The same authors published a photo receptaculids, in which the stellate plates were over graph of a “speculate sponge” from the Vendian of the time replaced by solid rhomboid plates (Zhuravlev, White Sea Region, which is possibly a stalked vendo 1986). biont similar to Palaeophragmodictya spinosa Botting and Butterfeld (2005) collected interesting described in the same locality by Serezhnikova (2007). material on heteractinids (fossil sponges) with skele The tube itself, which is a Palaeophragmodictya speci tons composed of regular multiradiate spicules (which men from Ediacara Hills (Gehling and Rigby, 1996), was the reason behind their assignment to a separate has a fractal structure of canals typical of Osmotro order within the Calcarea). The authors found in the pha–vendobionts rather than sponges that are suspen earliest heteractinid Eiffelia bilayered hexaradiate and sion feeders. Late Ediacaran spicules from the Tsagan tetraradiate spicules of several orders, in which the Olom Formation of Mongolia (Brasier et al., 1997) core is composed of highmagnesium calcite and the were shown to be inorganic mineral crystals (Antcliffe external layer is composed of silica (opal) (Fig. 1). et al., 2011). It is difficult to imagine that the Ediaca Since the hexaradiate siliceous spicules are found only ran Coronacollina (Clites et al., 2012) was a sponge. It in hexaactinellids and calcite tertraradiate spicules are has a prefect tetraradial arrangement of spicules of the typical of the calcareous sponges, it was suggested that same number in differently sized specimens of this fos heteractinids were transitional taxa from Silicea to sil (from 1 to 22 mm across), which more likely sug Calcarea. This hypothesis was supported by phyloge gests a mineralogical origin. New spongelike organ netic analysis of microRNA (Sperling et al., 2010) and isms continue to be reported from ancient beds: e.g., also by the appearance of spicules in calcareous unusual, possibly skeletal remains from the Trezona sponges later in the fossil records than spicules of Formation (660–635 Ma) in South Australia (Maloof hexaradiate and common sponges (Zhuravlev and et al., 2010b) and Otavia in rocks from 760–635 Ma in Wood, 2008). Namibia (Brain et al., 2012), but the assignment of these fossils to sponges, or to the Metazoa in general, remains unsubstantiated. Cnidaria: Where the Jellyfish Swam? The sponge record begins in the Cambrian Period Most Ediacaran organisms have previously been with the appearance of Hexactinellida, Demospon considered members of Cnidaria, mainly jellyfish and giae, and Calcarea known from spicules of a certain sea pens (Octocorallia) (Glaessner, 1984; Jenkins, symmetry type and chemical composition, as well as 1992). However these “sea pens” are vendobionts, complete skeletons (Fig. 1). Only Homoscleromorpha whereas Ediacaran “jellyfish” represent vendobiont are not confirmed in the fossil record. In contrast, attachment discs or colonies of algae and/or bacteria there were several extinct groups of sponges in the (Grazhdankin and Gerdes, 2007; Serezhnikova, 2007, Cambrian Period: heteractinids and archeocyaths. 2013). Cambrian “jellyfish” were more diverse; some The latter were the most prolific and became largely of them were fossil traces (Jensen et al., 2002); brachi

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 426 ZHURAVLEV opods (Zhang et al., 2009); Xenusia (Ramsköld and attachment discs and pseudocolonies in the two latter Chen, 1998); paropsonemids; pelagic organisms with taxa suggests their cnidarian affinity. a multilobed, possibly chitinized, swimming disc, and The history of Cnidaria, like the history of suspended spirally coiled gut with a crown of branch Sponges, contradicts Dewel’s (2000) hypothesis that ing tentacles around the mouth; animals compared Bilateria could have evolved from clonal animals like with lophophorates and deuterostomes (Friend et al., sea pens, the colonial organization of which gave rise 2002; Zhu et al., 2002); and even the mouthparts of to the triblastic ancestors of Bilateria. Dewel consid extinct Ecdysozoa (Anomalocarididae) (Whittington ered sea pens to be Vendobiota, a fossil group that had and Briggs, 1985). Possible jellyfish imprints are no connection to the origin of Bilateria and Metazoa. known only from the Middle Cambrian (Young and If the fossil record is taken into account, the first fossil Hagadorn, 2010). Their affinity to any extant groups is organisms in each major branch of Bilateria—Ecdys not established, although statements to the contrary ozoa, Lophotrochozoa and Deuterostomia—repre can be found in the literature. For instance, Cart sent the remains of of nonclonal organisms capable of wright et al., 2007, based on 120 specimens, described movement. Moreover, even among confirmed fossil jellyfish representing three modern classes and four fam sponges and cnidarians, all of the earliest representa ilies (Hydrozoa, Scyphozoa (2), and Cubozoa). How tives are solitary organisms. For instance, a represen ever, all four have the same “umbrella” size (7–8 mm) tative statistical sample (all 305 known genera) of the and number of “tentacles” (about 18), whereas the earliest archaeocyaths were solitary organisms, and authors determined the presence of any diagnostic they only later gave rise to the first branching (modu characters from imprints of various preservation states lar) and, later, massive (multimodular) taxa (Wood et or the position on the bedding surface. In other words, al., 1992). The term “modular” is used here because this is either a species combining characteristics of all all colonial organisms are modular, i.e., they consist of three modern classes or not a jellyfish at all. modules, but not all modular organisms can be con sidered colonial. For instance, in most archaeocyaths, The earliest Cnidaria, with mineral and chinitized the modules are separated by secondary skeletal skeletons, appear only in the Cambrian Period, i.e., at deposits that in the live animal gradually lost their con least 30 Ma earlier than the aforementioned Middle nection to one another, even if they developed by Cambrian “jellyfish”. They were at first very simple branching or budding from the same paternal individ singular organisms; after 10–15 Ma, they were modu ual. The same applies to the Cambrian speculate lar forms similar to Ordovician corals (Tabulata) sponges (Hexactinellida, Demospongiae, Calcarea). (Zhuravlev et al., 1993; Zhuravlev, 1999; Fuller and The solitary forms are the first to appear in the fossil Jenkins, 2007; Park et al., 2011) (Fig. 1). Apart from record, and only much later do very rare modular taxa these, the possible Cnidaria included Hexaconularia appear. Their complete skeletons, not disassociated (sessile organisms with phosphatic (or postmortem into separate spicules, are found in Lagerstätten and phosphatized) skeletons in the shape of an upturned lithified reefs (Rigby and Hou, 1995; Rigby and Col hexagonal pyramid), which are only known from the lins, 2004; Ivantsov et al., 2005; Kruse and Zhuravlev, basal Cambrian of South China and India, and conu 2008; Wu et al., 2014). In general, of the 4367 genera lariids with a fourfold organic, or probably chitinized, of Cambrian fossil organisms known by 2001, only skeleton covered on the top. Conulariids appeared in 3.5% are modular taxa (archaeocyaths, radiocyaths, the Late Cambrian, and hexaconoluriids are com and other sponges—75 genera; coralomorphs—25; pared to Stauromedusae, if tetraradiate symmetry is bryozoans—2; graptolites and pterobranchs—48) considered as a major character, or with Coronata, if (Wood et al., 1992; Zhuravlev, 2001). In the last strobililike constrictions are taken into account decade, another 400 genera were described, of which (van Iten et al., 2006, 2010). Hexaconularia include no more than 5 are modular, so their total proportion some Cambrian embryos known as Punctatus and decreased. None of these taxa is an early ancestor of Olivoodes and resemble juvenile coral polyps included any group of Metazoa. in the peridermis (Bengtson and Yue, 1997; Dong et al., 2013). However, some Olivoodes and “soft corals” have a pentaradial symmetry instead of tetraradial, as Deuterostomes well as micrornamentation, which does not exclude (With and without Inverted Commas) their possible affinity to Ecdysozoa (Liu et al., 2014; Although a third of Cambrian modular organisms Steiner et al., 2014). The same group of jellyfish pre were hemichordates, the earliest Deuterostomia were sumably includes the hyolithelminthes Byronia and not colonial organisms. Among hemichordates, pter Sphenothallus, represented by phosphate tubes with obranchiates appeared only inthe Middle Cambrian, transverse ribbing and microlamellar microstructure and the earliest of these are very simple solitary taxa— common in the Cambrian rocks (Bischoff, 1989; “Rhabdopleura” and Cephalodiscus(?) (Durman and van Iten et al., 1992; Zhu et al., 2000; Vinn, 2006). Sennikov, 1993; Harvey et al., 2012). Their aggrega These are often compared with annelids or pogono tion presumably resulted in the appearance of simple phores, but their microstructure and the presence of colonial organisms (Maletz, 2014). A further increase

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 427 in the complexity of blastogenesis occurred in grapto Problematic genera assigned to chordates (Pikaia, lites (Cooper et al., 1998). The pterobranch affinity of Metaspriggina, Yunnanozoon, Cathaymyrus, Haik all these taxa was established based on the morphology ouella, Myllokunmingia, Haikouichthys, and of the tubular organic skeleton, which in pterobranchs Zhongjianichthys) appear in the Lower and Middle (coenecium) and graptolites (rhabdosome) is com Cambrian–Chengjiang and Burgess Shales, respec posed of collagen fusellar layers (Mierzejewski and tively (Chen et al., 1995a, 1999; Shu et al., 1996, 1999, Kulicki, 2001). 2003a; Shu, 2003; Conway Morris, 2008; Conway The problematic earliest Cambrian pterobranchs, Morris and Caron, 2012). Yunnanozoon and Haik Galeaplumosus and Herpetogaster, represent imprints ouella, as well as Myllokunmingia and Haikouichthys, of solitary organisms with crowns of feathery tentacles apparently represent different forms of preservation of and without a coenecium (Caron et al., 2010; Hou the same taxa; and the differences between them are et al., 2011). Their pterobranch affinity is not con not greater than of species level (Hou et al., 2002; firmed, because the zooids of pterobranchs degrade Chen and Huang, 2008). The Middle Cambrian within a few days, losing all distinct characters of a Pikaia, which was the first of the fossils to be inter class or even a phylum (Briggs et al., 1995). In addition preted as a chordate, has antennalike appendages in the tentacles of modern pterobranchs develop from a the head region and almost flat borders of the myo mesosoma, or collar, rather than from the prosoma, or tomes, which suggests the absence in this taxon of a head shield (anterior region), where they occur system of muscles typical of chordates (Lacalli, 2012). (Maletz, 2014). In contrast, Yunnanozoon, despite the presence of a The two Middle Cambrian fossils, which were pre segmented dorsal crest, strongly agrees with the body viously assigned to annelids or priapulids, Oesia and plan of this phylum: the crest, which resembles a V Spartobranchus are more interesting. Their large (up shaped myosepta, could be an additional support for to 10 cm) wormlike body with a straight gut is subdi muscle blocks, reducing the load on the myosepta and vided into three regions. The second possesses numer thereby facilitating active swimming movements ous gill slits, whereas the mouth opening in Sparto (Lacalli, 2012) (Fig. 1). Although Cambrian fossils, branchus occurs at the border of the head and neck which are described as chordates, are difficult to inter regions, and the head region contains structures pret, the number of Yunnanozoon specimens reaches resembling a stomochord and “Yshaped structure” many hundreds, and therefore, despite taphonomic (Conway Morris, 2009; Caron et al., 2013a) (Fig. 1). distortion (making it impossible to establish the pres However, it has an external organic tube embracing ence of a notochord), it is possible to assume reliably about a quarter of the organism’s length, which some the presence in this group of Vshaped myotomes, gill times branches. This tube could be ancestral to the slits connected with the gut, gill arches, paired gonads, coenecium of pterobranchs. The sistergroup rela and a postnatal caudal region, which indicates a chor tionships of Pterobranchia and Enteropneusta are date affinity (Shu et al., 2003b, 2010; Donoghue and suggested by molecular and comparative anatomical Purnell, 2009; Lacalli, 2012). This is supported by evidence (Brown et al., 2008; Swalla and Smith, 2008; experiments on postmortem changes in the remains of Philippe et al., 2011), which does not exclude the pos modern Cyclostomata and other chordates (Sansom et sibility of the Pterobranchia having evolved from al., 2011). Although the features of Yunnanozoon, as Enteropneusta. well as Cathaymyrus and Metaspriggina known from individual specimens, agree with the body plan of As for the occurrences of the Early Cambrian chor cephalochordates, , with its dorsal dates, the presence in the presumed tunicates ( Myllokunmingia Che and ventral fins and nasal capsules, can be considered ; Shu et al., 2001; ungkongella, Phlogites, Shankîuclava the earliest chordate (Hou et al., 2002; Conway Mor Chen et al., 2003) of tentaclelike structures is most ris, 2008; Shu et al., 2010). The remains of the little similar to the body plans of tentaculate animals known (Shu, 2003) are unfortunately (Caron et al., 2010; Shu et al., 2010). It is quite possi Zhongjianichthys too incomplete to make any hypotheses of its affinity. ble that the “softbodied pterobranchs” and “tuni cates” are the remains of tentaculate animals pre Odontogriphus from the Burgess Shale, despite served due to chitinization of their external covers: the recent attempts to assign it to the softbodied mol “tunicates” strongly resemble Cambrian brachiopods lusks, possibly belongs to the Cambrian Deuterosto with a nonmineralized shell (they have structures like mia (Caron et al., 2006; Conway Morris and Caron, a pedicle, shells, and the lophophore), whereas Herpe 2007; Smith M.R., 2012). It needs to be noted that, of togaster is distinguished from the paropsonemids dis all Molluscan features, this taxon has only a mouth cussed in the previous section only in the absence of a opening surrounded by teeth, which are compared to swimming disc. Interestingly, Cheungkongella has pre a radula, whereas its body, with a pronounced trans viously been considered a hypothetical pentaradiate verse segmentation, does not correspond to this plan ancestor of chordates, although its poor state of pres (Conway Morris, 1976; Butterfeld, 2006). This mor ervation and the absence of the side presumably with phology of Odontogriphus could equally suggest an the mouth opening, do not allow any considerations of affinity to chordates; as with Yunnanozoon, this is sup its symmetry. ported by a type of preservation not typical for mol

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 428 ZHURAVLEV lusks. This similarity was recently emphasized by annelids and arthropods (Arendt and NublerJung, Smith (2012), who studied 165 specimens of mouth 1994; Brown et al., 2008; Lowe, 2008; Nomaksteinsky apparatus of Odontogriphus and made significant argu et al., 2009). The new (“dorsal”) mouth opening in ments as to why this fossil cannot be an annelid: the modern Amphioxus opens in place of a gill slit (Benito multirowed mouth apparatus, the presence of a basal Gutierrez and Arendt, 2009), but the mouth was membrane, and the probability of supporting appara almost terminal rather than ventral in the Cambrian tuses. One important observation listed by Smith (but Yunnanozoon (equivalent of Amphioxus). not discussed, as he considered Odontogriphus to be a In a sense, the subdivision of Bilateria into pro mollusk) shows that this animal could not be a mol tostomes and deuterostomes lost its usefulness, lusk: the tooth cavities contain increased concentra because, even in Priapulida, the blastopore gives rise to tions of Ca and F, which are absent elsewhere in the the anus at the vegetal pole, following strictly a deu body. This means that the teeth in Odontogriphus were terostomic pattern. Moreover, the succession of calciumphosphate, like the teeth of chordates. expression of regulatory genes during the formation of The latter include the multiple phosphate teeth of the blastopore, mouth, and anal opening is the same in conodontophorides, which (conodonts) were wide priapulids and deuterostomes (MartínDurán et al., spread from the Middle Cambrian up to the Triassic 2012). Period. Only three Paleozoic localities contain In total, the paleontological and molecular data, as imprints of the conodontophoride body. The imprints well as embryological studies, suggest that tunicates reveal large eyes, complex tooth apparatus, gill slits, V were not a group that evolutionarily preceded cepha shaped myotomes, and a tail with a caudal fin (Ald lochordates or even vertebrates. It is possible that they ridge and Briggs, 1986; Donoghue et al., 2000) (Fig. 1). are secondarily simplified; they lost some of their However, the teeth are most important to understand Hoxgenes and, along with them, nephridia and traces the affinity of these animals. The teeth have three lay of metamere structure (Delsuc et al., 2006; Brown et ers, including enamel and dentine, suggesting that al., 2008; Putnam et al., 2008; Cannon et al., 2009; they belonged to jawless vertebrates, most likely active GarcíaFernàndez, BenitoGutiérrez, 2009; Smith A., predators (Barskov et al., 1978; Donoghue, 2001; 2012; Caron et al., 2013a; Maletz, 2014). Whatever Goudemand et al., 2011; Nemliher and Kallaste, place the Cambrian chordates might have occupied 2012). among deuterostomia, primitive cephalochordates, or It is thought that the notochord in Yunnanozoon, vertebrates, they were solitary (nonclonal) motile nek Cathaymyrus, and Myllokunmingia occurs on the dor tonic or nektobenthic organisms. Moreover, the pres sal side, above the gut (Chen et al., 1999; Shu et al., ence of the phosphate inner skeleton in vertebrates 1999). However, it is difficult to determine positively indicates that their ancestors were motile and very which fossil structures correspond to this organ. The active animals, because high muscle activity results in Yunnanozoon has a rodlike structure under the gut a decrease in pH in the inner medium of the organism which is not thought to be a notochord, because “the up to the level at which only the phosphatic skeleton purported yunnanozoan notochord is in a ventral remains insoluble (Ruben and Bennett, 1987; Wood position where it could not act as an antagonist” (Shu and Zhuravlev, 2012). If the first chordates were poor and Conway Morris, 2003, p. 1372d). However, to swimmers like Amphioxus, their skeleton would have interact with the muscles, Yunnanozoon had a seg to be built of energetically more efficient carbonate, mented crest, whereas the notochord could also have like echinoderms. functioned in the same way, if it was in the dorsal posi Cambrian echinoderms can easily be recognized, tion. Indeed, this organ could not have shifted by even from separate plates with a stereomic structure itself, whereas the cephalochordates could have had it, that is found only in this phylum and always consists of as was shown by Malakhov (1977), judging from the highmagnesium calcite. Four main groups are recog behavioural features of Amphioxus (cephalochordate) nized among these echinoderms based on the body and the fact that the body plan of Enteropneusta plan and the presence of ambulacra: (1) bilaterally exactly mirrors that of Chordata (position of the pro symmetrical, without ambulacra (Ctenocystoidea); tocoel, coelomic openings, neural plate, blood flow (2) asymmetrical, both with and without ambulacra direction, and incipient blastopore). Geoffroy Saint (Cincta, Soluta, and Stylophora, also known as Car Hilaire (1822) tried to prove the same hypothesis, but pozoa); (3) spirally symmetrical, with numerous 190 years ago he could not refer to the evidence pro ambulacra radiating from the mouth opening (Helico vided by molecular biology. Data on the expression of placoidea); and (4) pentaradial with a pentaradial regulatory genes in the ontogeny of the nervous system arrangement of ambulacra (Edrioasteroidea, Rhomb and “general marker genes ” during gastrulation (in ifera and Eocrinoidea sensu lato) (Zamora and Smith, vertebrates Chd marks the dorsal side and BMP4/2 2012; Smith et al., 2013). Early Cambrian echino marks the ventral side, and their orthologs in insects, derms include taxa with perfect bilateral symmetry Sog and Dpp, vice versa mark the ventral and the dor (Ctenoimbricata, Courtessolea) that are morphologi sal sides) confirmed that the dorsal neural cord of ver cally intermediate between the classes Ctenocystoidea tebrates is homologous to the ventral neural chain in and Cincta, which some authors consider basal for all

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 429 echinoderms; the periproct and the anal pyramid in Aldridge et al., 2007; Shu et al., 2010; Vinther et al., these taxa occur on the posterior end of the body, indi 2011; Ou et al., 2012a). These remains can be inter cating a straight rather than Ushaped gut (Zamora preted differently: a carapace with cellular ornamen et al., 2012) (Fig. 1). Occurrences in the Middle Cam tation and a segmented tail (Briggs et al., 2005; Caron, brian of Spain and France of juvenile Cambraster from 2006; Bergstrom, 2010; Zhuravlev et al., 2011b) (Fig. 2j). the class Edrioasteroidea show that these perfectly In the former case, the resulting organism had the pentaradial attached echinoderms in early ontogeny characteristics of a chordate and hemichordate but retained bilateral symmetry (Zamora et al., 2013, fig. 7). with a segmented tail. In the latter case, it had the Edrioasteroidea are considered a likely stem group for characteristics of a legless arthropod. The latter have all Eleutherozoan echinoderms (starfish, sea urchins, cellular carapaces and a thin folded structure (Butter sea cucumbers, and brittle stars) (Rozhnov, 2012). feld, 2002). Even when this description is supple These paleontological data are supported by molecu mented by another important characteristic, i.e., a ter lar biology: echinoderms retain the ancestral complex minal mouth opening with cyclically arranged tooth of genes characteristic of a bilaterallysymmetrical plates, this will not clarify the problematic affinity, body plan similar to that in an ancestor shared by all although the hypothesis of the deuterostome affinity of deuterostomes, whereas the similar larva—dipleurula, Vetulicolia and Banffozoa seems to be not very consis along with molecular data, allows their consideration tent. These animals cannot be assigned to arthropods, as a sister group of hemichordates within the Ambu since they lack a key feature. Perhaps these were early lacraria (Morris, 2007). members of Ecdysozoa, which could include only Pentaradiality (or simply radiality), a key character partly segmented animals like anomalocaridids, which of the echinoderm phylum, is absent in many early are different from Vetulicolia only in the presence of echinoderm taxa. These can be recognized from the mouthparts and compound eyes. stereome structure of skeletal elements resulting from highly cooriented mineral nanoparticles formed from amorphous precursors of highmagnesium calcite. Ecdysozoa: Abundant Fruit of Arthropodization They give the optical qualities of a single crystal to the The concept of arthropodization, which was ele entire porous element (Killian et al., 2009). Since the gantly used by Ponomarenko (1998, 2004), aptly skeletons of chordates and echinoderms were funda explains the main evolutionary processes of the Cam mentally different from the very beginning of these brian Period: segmented appendages (arthropodiza groups, the old and now forgotten calcichordate cla tion s.s.) and carapaces (arthrodization) indepen distic hypothesis, according to which chordates dently appear not only in arthropods (probably more evolved from asymmetric Cambrian echinoderms than once) but also in anomalocaridids, some xenu (Carpozoa) (Jefferies, 1986), was shown to be unsub sians, and vetulicolians. These animals, along with stantiated. Cladistics helps very little to interpret pale their wormlike relatives, essentially cleared Canfield’s ontological material, because in this case it is impossi ocean due to bioturbation, the establishment of a fecal ble to analyze hundreds and thousands of homologous pellet conveyor belt, and the creation of a multitiered equally weighted characters (as in molecular biology trophic pyramid with predators of several orders. They or in structural linguistics). Therefore, the composi eventually made it suitable for life in all its diversity. tion of the stem and terminal groups significantly Unsurprisingly, the remains of Ecdysozoa, as men changes in each new cladogram (see Wills, 1995; Legg tioned above, constitute 70% of Cambrian fossils in et al., 2012, 2013). Nevertheless, a series of terms used their diversity, number of individuals, and biovolume, in cladistics, for example “synapomorphy,” “stem,” thereby comprehensively representing their evolution. and terminal groups, turn out to be more useful than Although many zoologists still think that the con “ancestors” and “descendants” to characterize fossils cept of the generalized “body plan,” hard won by cen of a higher rank that do not fit the framework of phyla turies of comparative anatomy studies, is undermined and classes outlined in the modern material, e.g. Cam by phylogenies based on molecular data, this is far brian echinoderms. from true. The “centuriesold tradition” was discon Along with echinoderms, hemichordates, and tinued with the development of completely new tech chordates, the Cambrian Lagerstätten often contain nology of molecular studies but also by technology the remains of one or two other groups, Vetulicolia and allowing insight into the smallest living organisms at Banffozoa (named after the typical genera Vetulicola any stage of their evolution and their fossil remains. and Banffa), which are lately assigned to Deuterosto Therefore, a revision of previous concepts about the mia and, more precisely, to chordates. These organ relationships between the phyla and classes also isms, which are a few centimeters in length, are occurred in modern morphological, embryological, described as a bilaterally symmetrical and clearly sep and paleontological research. Interestingly, the idea to arated into an anterior section covered by a carapace, connect nematodes and arthropods (insects) is not with gill slits opening into the gut, and with filaments, new, and, despite common belief, it was not put for endostyle, and a dorsal fin, whereas the posterior end ward by molecular biologists. It was Odo Reuter (a has the appearance of a segmented tail (Gee, 2001; Finnish entomologist) who was the first to note the

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 430 ZHURAVLEV similarities in the chitinous covers, absence of cilia, Such an epithelium develops in Lophotrochozoa, and reduced ability to regenerate, and the absence of the the cuticle in this group is never molted entirely but is ring muscle in these groups (Reuter, 1913; Lyubish replaced in patches (SchmidtRhaesa et al., 1998). An chev, 1982). Reuter can be considered the pioneer of ecdysozoanlike cuticle is present in at least two Cam the ecdysozoan hypothesis. brian groups: Palaeoscolecida (primitive cephalo The Ecdysozoa has three important characters rhynchs) and xenusians (onychophoranlike organ (synapomorphies): embryonic development, structure isms with terminal position of the mouth opening) of the cuticle, and, to some extent, the morphology of with phosphatized culticular layers. Collagen fibers are the mouth apparatus. It is worth noting the his of course absent in fossils, but numerous cavities that tochemical similarity of the nervous system of Ecdys housed them are distinctly visible (Zhuravlev et al., ozoa (arthropods, onychophorans, priapulids, nem 2011b). Larval sheaths are known in various fossil atomorphans, and nematodes), revealed in the similar cephalorhynchs, xenusians, and arthropods, some of expression of components during immunohistochem which were buried during molting (Müller and Hinz ical staining by certain ferments, which do not cause Schallreuter, 1993; GaríaBellido and Collins, 2004; similar reactions in cnidarians, ctenophores, annelids, Topper et al., 2013b). mollusks, rotifers, chaetognaths, bryozoans, or deu The radial symmetrical retractile proboscis (intro terostomes (Haase et al., 2001). vert) is a very important organ, which, apart from the Ungerer and Scholtz (2009, p. 272) considered that nervous center, includes a system of retractory muscles new studies of the embryonic development of pyc and has numerous concentric rows of hollow sensory nogonids, as well as arthropods (Alwes and Scholtz, locomotory spines (scalids). The introvert, which is 2004), tardigrades (Hejnol and Schnabel, 2005), nem used for orientation, searching, and grasping food, atodes (Schulze and Schierenberg, 2008), priapulids and locomotion, is present, at least at the larval stage, (Wennberg et al., 2008), and kinorhynchs (Kozloff, in the Priapulida, the Loricifera, the Kinorhyncha, 2007), reveal “… holoblastic, irregular radial, regular and the Nematomorpha (which Malakhov (1980; to nearly regular cleavage and a gastrulation specified Malakhov and Adrianov, 1995) included in the phylum by large divisionretarded immigrating blastomere fol Cephalorhyncha and Nielsen included (1995) in the lowed by smaller immigrating blastomeres.” This type Introverta (including the Nematoda) (Eriksson and of embryogenesis was likely to be initial for all Ecdys Budd, 2001; Liu et al., 2014)). Some pycnogonids also ozoa lacking spiral cleavage, ciliated larva, or a larva possess an introvert (Nielsen, 1995), while pyc with an apical plate or apical tuft. nogonids have a nonretractable proboscis and a trira The cuticle of Ecdysozoa is composed of laminate diate pharynx typical of some cephalorhynchs and epicuticle secreted by the microvilli of epidermal cells nematodes (Eriksson and Budd, 2001b; Liu et al., and the protein exocuticle and endocuticle composed 2014). There are also fossil Jurassic pycnogonids with of αchitinous fibers, which are assembled in spiral a hypertrophied proboscis (Charbonnier et al., 2007). plates. A complete change of the cuticle (molting) Tardigrades have a prominent telescoping mouth cone occurs at least once in the lifetime; it is induced by ste surrounded by a ring of platelike peribuccal lamellae roid hormones (ecdysones), as was demonstrated for that resembles a kinorhynch mouth cone and a tri onychophorans, tardigrades, arthropods, priapulids, radial buccopharyngeal apparatus armed with teeth kinorhynchs, loriciferans, and nematophorans (Robson, (Dewel, R.A. and Dewel, W.S., 1997; Kristensen, 1964; Crowe et al., 1970; Plotnick, 1990, Schmidt 2002; Dewel and EibyeJacobsen, 2006). A nonre Rhaesa et al., 1998; Lemburg, 1999; Nielsen, 2001; tractable proboscis and introvert are also found in var SchmidtRhaesa, 2006; AlSawalmih et al., 2008). ious groups of Cambrian cephalorhynchs, xenusians, The formation of the cuticle, like molting in Ecdyso and anomalocaridids (Hou et al., 2006; Gamez Vin zoa, is controlled by the same group of regulatory taned et al., 2011; Zhuravlev et al., 2011b); in the lat genes of the hormonereceptor NHR23 complex ter, the mouth cone is triradiate (Daley and Edge (Kouns et al., 2011). Although the cuticle lacks chitin combe, 2014). in adult nematophorans, αchitin fibers are present in Modern data on the ontogeny of onychophorans the basal layer of the larval cuticle, as in the lorica of show that the larval mouth begins as terminal, whereas the priapulid and loriciferan larvae (Neuhaus et al., the antennae and jaws develop from incipient legs and 1996); in nematodes, the αchitin cuticle is preserved the jaws are homologous to terminal claws. The in the pharyngeal region (Neuhaus et al., 1997). In appendages also give rise to slime papillae, which are annelids, the cuticle is totally different: its layers are revealed by the presence of transient nephridial formed by collagenous cords composed in a quasior anlagen (nephridia are absent in adults). The excretory thogonal lattice penetrated by numerous protuber channels of these nephridia at the antenna and jaw ances of epithelial cells; it lacks chitin. βchitin is base are closed, although they retain ciliated epithe present only in setae; mollusks, brachiopods, and bry lium, and these are transformed into slime glands in ozoans have γchitin (Plotnick, 1990). The thick the pair of slime papillae (Eriksson et al., 2003; Mayer molting cuticle of Ecdysozoa precludes the develop and Koch, 2005; Strausfeld et al., 2006). The mouth ment of any kind of ciliated epithelium, even in larvae. development in adults and the initial growth and pri

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 431 mary innervation of the antenna remain unresolved. At present they are assigned to several extinct Some authors studying onychophoran embryogenesis classes of cephalorhynchs that differ in the head region consider that the ventral mouth in onychophorans is morphology (introvert or nonretractable proboscis), embryologically terminal and that the antennae the presence or absence of the neck, and the morphol develop from legs and are innervated by the protocer ogy of the sensory glands (Conway Morris and Robi ebrum (Eriksson et al., 2003). Others think that the son, 1986; Malakhov and Andrianov, 1995; Hou et al., mouth is formed anew by shifting derivative labial 2006; Maas et al., 2007; Harvey et al., 2010; Zhuravlev papillae of the antennae, jaw, and third segments, et al., 2011b; Liu et al., 2014). There are confirmed whereas the antennae are innervated by deuterocere records of burrows of Cambrian cephalorhynchs con brum (Ou et al., 2012b). Martin and Mayer (2014) taining buried remains of inhabitants that are some showed that onychophoran antennae are innervated times identifiable by species (Zhang et al., 2006; by the protocerebrum and are hence homologous to Zhuravlev et al., 2011b; Huang et al., 2014): these are the crustacean labrum, which starts as a paired organ simple Ushaped burrows (Fig. 2a) or deadend, sac as a result of the expression of the regulatory Distal like burrows similar to those inhabited by extant pri less gene (Browne et al., 2005; Kimm and Prpic, apulids and completely unlike false traces Treptichnus 2006). pedum common in the basal Cambrian, which have Based on the onychophoran ontogeny, the ances been interpreted as priapulid burrows (Vannier et al., tral taxon of this group can be interpreted as a vermi 2010). Thus, there is no evidence suggesting that form organism with paired retractable undifferenti cephalorhynchs preceded xenusians. The latter are ated lobopodia and proboscis and with a terminal known from beds over 525 Ma as larval skins (Xenu mouth. Such organisms present as one of the common sion; Dzik and Krumbiegel, 1989) and from beds older Cambrian ecdysozoan groups, which are assigned to than 535 Ma as phosphatized claws and cuticular Xenusia, Tardipolypoda, or simply animals with spines, whereas the first confirmed cephalorhynchs lobopodia (Dzik and Krumbiegel, 1989; Budd, 1998; (Palaeoscolecida) appeared no earlier than 525 Ma Gamez Vintaned et al., 2011; Ou et al., 2012b). This (Zhuravlev et al., 2011b; Caron et al., 2013b). The lar group includes the famous Hallucigenia, which was vae of priapulids, loriciferans, and nematophorans, originally described upside down and back to front; in and even their adults, retain characters of palaeoscole fact the paired spines are on the back, whereas the cids and their larvae in the structure of the cuticle flexible appendages are paired walking limbs. (Maas et al., 2009; Peel, 2010). Kinorhynchs, although not found as fossils, have a serial arrange However, xenusians include species with a retract ment of muscle facies associated with the cuticular able proboscis, as in cephalorhynchs, and with segments and a mouth cone like that in Cambrian appendages clearly unsuitable for locomotion but suit cephalorhynchs (Omnidens). Reverse evolution— able for anchoring in holes (Mureropodia) (Gamez from cephalorhynchs to xenusians and arthropods—is Vintaned et al., 2011) (Fig. 2b), burrowing organisms adhered to by almost all authors (Dzik and Krumbie (Facivermis) with anterior lobodialike appendages gel, 1989; Budd and 2001; Zhang and Briggs, 2007; and a vermiform posterior region (Liu et al., 2006). In Daley et al., 2009; Liu et al., 2011; Legg et al., 2013) other words the posterior body and caudal segments in and is just a reworking of the annelidarthropod these animals were identical to those in Palaeoscole hypothesis. The transformation of a highly specialized cida (earliest cephalorhynchs). Palaeoscolecida were introvert into the simple mouth of xenusians and of the abundant in the Cambrian and became extinct in the sensory glands (papillae) into the locomotory append Silurian and were different from other cephalorhynchs ages of cephalorhynchs, which needed to be able to in the phosphatized cuticle composed of plates orga escape somehow from their burrows onto the sub nized in repeating transverse rows similarly morpho strate, is impossible biomechanically: the locomotion logically organized and structured to those in xenu of such worms by hydraulic pumping and coelomic sians (and onychophorans, although in the latter the fluid distribution is only suitable to move within the cuticle is not phosphatized). Some Palaeoscolecida substrate. The evolution from worms with a retractable retained reduced paired lobopodia on the ventral sur proboscis to onychophoranlike organisms is not in face, which probably became sensory glands (tubules agreement with the data on the brain ontogeny in ony and papillae) as in extant priapulids (Müller and Hinz chophorans: it has been shown that their brain is not of Schallreuter, 1993; Zhang and Pratt, 1996; Zhuravlev circumpharyngeal origin (Eriksson et al., 2003) but et al., 2011b) (Fig. 2a). begins as paired dorsal ganglia, the protocerebral part Cephalorhynchs with priapulid characters begin to of which innervates the antennae and eyes and the occur in deposits 520 Ma (nearer the end of the Early deuterocerebral part innervates the jaws, whereas the Cambrian) (Fig. 1). Many authors still refer to all fossil tritocerebrum is not formed (Strausfeld et al., 2006; cephalorhynchs as “priapulids,” although they have a Martin and Mayer, 2014). Based on the presence of completely different cuticle and mouth apparatus; antennae and eyes in some xenusians, it is possible to these taxa include gigantic animals with a mouth more suggest that the brain of xenusians with a nonretract than 0.2 m in diameter (Omnidens). able proboscis was similar.

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Xenusians represent a stem group not only for cladograms in which they are placed between xenu cephalorhynchs and onychophorans. Tardigrades are sians and true arthropods (Euarthropoda) (Budd and also their possible descendants; they are adapted to Telford, 2009). First, they lack the definitive charac meiobenthic habitats and thus have acquired a simpli ters of arthropods, apart from the preoral—append fied system of inner organs while retaining the initial ages that are not always segmented and compound morphology of lobopodlike appendages with claws eyes. Second, the mosaic combination of characters in and cuticle. Tardigrades stylets are derivatives of the various species of anomalocaridids and xenusians lobopodlike limbs that were transformed into inner crushes all cladistic schemes. For example, among organs (Dewel and EibyeJacobsen, 2006; Halberg xenusians, Diania have strongly cuticularized, almost et al., 2009), resulting in the bilateral appearance of segmented appendages and a head region without triradiate mouth apparatus. The transformation of the traces of a tagmosis and with a welldeveloped probos muscles from one complex of longitudinal and trans cis (Liu et al., 2011; Ma et al., 2014) (Fig. 2d). On the verse muscles to the serial fascia, which connects the contrary, Antennacanthopodia had lobopodlike limb to the cover plates, is observed in the Cambrian appendages with claws and a head region with traces of xenusians Hadranax and Pambdelurion (Budd, 1998, tagmosis and a reduced proboscis (Ou et al., 2011) 2001) (Fig. 2f), whereas the earliest Middle Cambrian (Fig. 2e), whereas Mureropodia has an introvert and tardigrade has paired rudiments of the lobopodian reduced lobopodlike appendages with claws appendages in the head region, in addition to four (Zhuravlev et al., 2011b) (Fig. 2b). Arthrodization and pairs of locomotory limbs and Cuticular plates like arthropodization did not necessarily occur together those in xenusians (Maas and Waloszek, 2001). This but instead developed independently in several groups process is connected with the functional differentia of Ecdysozoa (Ponomarenko, 2008; Mounce and tion of limbs and apparently with the transformation Wills, 2011): xenusians, anomalocaridids, vetulico of the ventral nervous cords into the segmented and lians, and partly tardigrades. later ganglionized ventral chain (Whittington and Kinorhynchs are worth mentioning again Mayer, 2011). (SchmidtRhaesa and Rothe, 2006). The origin of Another group likely to be associated in its origin Pycnogonida is not certain (whether they are true with xenusians—anomalocaridids (Anomalocaris, arthropods, closely related to chelicerates, or acquired Peytoia, Amplectobelua, and others)—are the largest a segmented skeleton independently), because fossil inhabitants of the Cambrian seas, up to one meter long Cambrian and Jurassic taxa have features of organiza (Figs. 2g and 2i). They have a proboscis with radially tion of the head section like those in xenusians arranged tooth plates, sometimes of several orders, as (Waloszek and Dunlop, 2002; Charbonnier et al., in cephalorhynchs (radiodonts or dinocarids); a pre 2007). The Early Cambrian arthropods Fuxianhuia oral pair of segmented or lobopodlike lobe grasping and similar taxa had the most simple plan of the head appendages, as in some xenusians; large compound region but with true antennae, a second specialized eyes (up to five in number), similar to the optical pair of segmented appendages and differentiation of organs of the most derived arthropods; a head shield the ventral somite into sternites and tergites, undiffer sometimes composed of several elements; a body with entiated cylindrical walking limbs with numerous swimming lobes possibly bearing respiratory fila smooth podomeres, and a rounded distal segment ments; and a caudal region with or without cerca and (Chen et al., 1995b; Bergström et al., 2009; Ma et al., a straight gut with serial paired digestive diverticulae 2012; Tanaka et al., 2013; Yang et al., 2013), differing (Whittington and Briggs, 1985; Hou et al., 2006; from the lobopodlike appendages in the higher degree Zhang and Briggs, 2007; Daley et al., 2009; Paterson of sclerotization, approximately as in Diania Xenusia et al., 2011; Daley and Edgecombe, 2014). This group (Fig. 1). also accommodates Opabinia and Nectocaris, which The presence of the coelom in arthropods and ony had been erroneously considered to be the earliest chophorans does not contradict the original position cephalopod, and chordates with a head shield, oral of xenusians as the ancestral group of Ecdysozoa, proboscis, paired preoral appendages, and external gill including cephalorhynchs (Eriksson et al., 2003; filaments (Fig. 2h). Anomalocaridids with preoral SchmidtRaesa, 2006), because a reduced coelom appendages, which were most likely to be innervated near the anterior gut is found also in priapulids (Meio from the protocerebrum, can be considered descen priapulus; Storch et al., 1989). Apart from that, the dants of xenusians that adapted to nektobenthic active distinct axial position of the gut in xenusians, predation and active filtration, based on the mouth palaeoscolecids, and some other Cambrian cephalo apparatus and in some taxa (Kerygmachela and Tami rhynchs suggest the presence of a controlling structure siocaris), the preoral lobopod appendages (Bergström that is similar to the mesentherium and hence the and Hou, 2003; Hou et al., 2006; Daley and Peel, coelomic cavity (Zhuravlev et al., 2011b). 2010). Whether or not Articulata is a “natural ” group, the It does not seem correct to consider anomalocari labrum of arthropods develops as a paired organ rather dids, which were extinct in the Devonian Period, as than the homologous prostomium of annelids (Melni the basal group for arthropods, as is considered in the kov, 1970; Melnikov et al., 1992; Kimm and Prpic,

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2006), whereas the paired ventral nervous chains in Imprints of earlier annelids, such as Protoarenicola these two groups have different origins and are not from the Cryogenic and Ediacaran beds of North homologous to one another if the nervous system of China, were in fact remains of algae with siphonate onychophorans with ventral cords lacking ganglia and organization (their carbonized covers had the same aggregations of gangliose cells is considered to be a structure as associated algal thalli, while the “retract stem group for arthropods (Mayer and Harzsch, 2007; able pharynx” was the attachment disc (Dong et al., Whittington and Mayer, 2011). The similarity of both 2008; Butterfeld, 2009). groups appears to be determined by the fact that On the whole the fossil record of early annelids is arthropods, representing Ecdysozoa, and annelids, a good illustration of Westheide’s (1997) theory of the representing Lophotrochozoa, retained a certain set of origin of chaetae as external defense elements in characters of the common ancestor of Bilateria, motile epibenthic taxa. The first polychaetes, e.g., including the limbs (Balavoine and Adoutte, 2003; Canadia, had exactly this “horrent” look. Later, as Prpic, 2008; Williams et al., 2012). wormlike locomotion developed, the covers devel Nielsen (2003), who tried to retain a united Artic oped transverse gaps lacking chaetae determining the ulata (Annelida + Arthropoda) (to which he had to existence of external metamery. Struck et al. (2011) assign Cycloneuralia with kinorhynch (also cephalo and Struck (2013) studied the molecular phylogenet ics of annelids and noted that this group includes two rhynchs), like the intermediate change between distinct branches, Errantia and Sedentaria. The com arthropods and priapulids–nematodes), considers the mon ancestor of all annelids in these authors’ recon trochophore larva with a preoral crown of cilia (pro struction is a motilesegmented animal with devel totroch) a synapomorphy of all protostomes and also oped parapodia on metameres along the entire body noted its clear absence in arthropods and cycloneura (Struck et al., 2011, fig. 2). lians, i.e., in all Ecdysozoa(!). However, if the inter mediate forms between different groups of Ecdysozoa Other worms belonging to Lophotrochozoa are not found in the Cambrian. Although and in the fossil record are found in abundance, some Archaeogolfigia Cambrosipunculus from Chengjiang (Huang et al., forms, which could have been considered intermedi 2004) have already been suggested as representatives of ate between annelids and arthropods, are completely the terminal group of sipunculids, which Eibye absent in the beds (for example, if anomalocaridids Jacobsen and Vinther (2012) thought to be sufficient with a proboscis slightly resembling the axial pharynx evidence to reconsider the new system of annelids, was of some polychaetes were considered as such interme proposed by Struck et al. However, the fossils them diate forms, their swimming lobes would have retained selves do not provide sufficient evidence for either the the supportive setae necessary for the attachment of ory: it is not certain that tentacles were present in at muscle bunches of the locomotory system. Why would least one of four specimens in both genera, and the gut they then need to switch to an external attachment of does not show undulation curves characteristic of the same musculature to the external carapace?) sipunculids. Moreover, the body surface of these worms clearly shows scalides and sclerites like those in palaeoscolescids, and are also abundantly found in the Lophotrochoans: same bed in Chengjiang. The straight, “posterior” sec the only Skeletons in the Closet tion of the gut is in fact imprints of the retractory mus Annelids, or, more precisely, imprints of their cov cles of the introvert structures found in Palaeolescidae ers, are also found in the Cambrian beds, although (Zhuravlev et al., 2011b). The literature on the Edi they are a thousand times less common than cephalo acaran and Cambrian period still has references to the rhynchs. They are exclusively represented by the occurrence of Pogonophora. In fact these are ribbed remains of motile polychaetes with bifurcate parapo organic tubes of problematic sabelliditids, the micro dia (noto and neuropodia) (Conway Morris, 1979; structure of which is distinct from that of Pogono Conway Morris and Peel, 2008; Vinther et al., 2011) phora (Urbanek and Mierzejewska, 1983; Ivantsov, (Fig. 1); only one, not the earliest, annelid taxon, Per 1990). ochaeta, with thick, hooklike setae was probably not It is interesting that, among the Ordovician–Car particularly motile (Merz and Woodin, 2006). None of boniferous annelids crawling on the surface of the sub the Cambrian annelids with their combination of strate, there were segmented taxa with calcareous characters can be assigned to any extant group: they elytra (Machaeridia) covering the parapodia with cha lack antennae, supporting chaetae, and dorsal or ven eta (Vinther et al., 2008; Vinther and Briggs, 2009). tral setae, and the palps are very simple (EibyeJacob The elytra of Machaeridia are similar to the shells of sen, 2004; EibyeJacobsen and Vinther, 2012). Scole Polyplacophora and diverse Cambrian “polyvalves” codonts (fossil jaws of polychaetes) appear only in the (Fig. 4e). It is not surprising that they were recently Ordovician beds, whereas reliable Sedentaria assigned to mollusks and to aplacophorans, which is appeared in the Mesozoic (tubes with a microstructure strongly supported by cladistics analysis (Sigwart and characteristic of annelids are found beginning from Sutton, 2007). the Triassic (Vinn, 2006; Vinn et al., 2008; Vinn and Diverse polyvalved taxa (Halwaxiida or Halkieri Mutvei, 2009). idae) are most interesting from the point of view of the

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 434 ZHURAVLEV origin of mollusks and other Lophotrochozoa. They integument, with the outer tuberculate layer mineral are united with Siphogonuchitidae in the order ized in the places of sclerite development and the inner Sachitida and with the order Chancelloriida in the underlying it and filling in the canals in the sclerites class Coeloscleritophora (Bengtson and Missar (Bengtson and Hou, 2001; Janussen et al., 2002). zhevsky, 1981). The complex external skeleton, or Cambrian sclerites of “polyvalves,” including scleritome, of these organisms, which developed on chancelloriids, typically with a thin inner organic layer the dorsal and lateral sides, is composed of numerous and a relatively thick middle layer, are composed of calcareous and/or organic sclerites and spicules of var primary aragonite fibers oriented along the axis of the ious shapes and one–two shells on the anterior and sclerite at a small angle to its surface, which deter posterior ends of the body resembling shells of brachi mined the scalelike ornamentation of the surface, opods or monoplacophorans (Fig. 4c). Apart from the and a thin external organic cover. The mineral layer above groups, Coeloscleritophora apparently include can be penetrated by canals (Butterfeld and Nicholas, Maikhanella and other Maikhanellidae, the cuplike 1996; Porter, 2008; Vinther, 2009). This microstruc shells of which consist of fused sclerites very similar to ture selection has no equivalent in true mollusks, but those of siphogonuchitids (Bengtson, 1992). The posi some features of the crosslaminated microstructure tion of all of these fossils within Lophotrochozoa and and scalelike ornamentation (apparently calcified their affinity to Wiwaxia, which has the organic scleri periostracum) in the shells of Maikhanellidae, which tome, is debatable. Some authors compared the large could be part of the scleritomes (they are only absent shells with those of brachiopods and other sclerites in Chancelloriidae), also point to the similarity of this with the elytra and chaeta of annelids, considering group to Mollusca, whereas the caplike protoconch is halkieriids and halwaxiids to be stem groups of similar to that of monoplacophorans (Feng et al., Lophotrochozoa as a whole (Conway Morris and Peel, 2003; Ponder et al., 2007). 1995; Holmer et al., 2002; Conway Morris and Caron, Interpretations of the earliest caplike and coiled 2007). Other authors, based on data on the sclerite Cambrian shells essentially varied; although they were structure (i.e., the presence of a complex system of assigned to monoplacophorans (Runnegar and Jell, canals connecting the interior cavity of a sclerite with 1976; Runnegar, 1996), gastropods (Golikov and Star its surface, that is indistinct from the canals penetrat obogatov, 1988) and to the extinct classes Helcionel ing chiton shells and housing the epithelial papillae loida and Paragastropoda, and occasionally to Rostro (estetes) and the mouth apparatus, which resemble conchia (Pojeta and Runnegar, 1976; Linsley and radula), consider them to be true mollusks preceding Kier, 1984; Peel, 1991), there was no doubt that these poly and aplacophorans (Scheltema and Ivanov, were indeed mollusks. Yochelson (1975, 1978) sug 2002; Vinther and Nielsen, 2005; Vinther, 2009; gested that such shells could belong to worms, but at Smith, 2012). Interestingly, even the hardest elements that time neither the microstructure, nor protoconchs of the same scleritomes, if their mineral composition is or muscle scars on these shells had been studied, and completely dissolved, show capillaries, as in the chae their general morphology was poorly described. tae of the synchronous annelids, e.g., Canadia (But Parkhaev (2004, 2008, 2014) and Ushatinskaya and terfeld, 1990, 2003, 2006). However, it is impossible to Parkhaev (2005), based on Parkhaev’s collection of simultaneously accept these chaetae as a synapomor ancient fossil mollusks, which is the largest in the phy of Lophotrochozoa or to consider their presence world, studied the muscle scars, microstructure, and as exclusive to annelids, as is thought by some authors protoconch with a septum separating it from the (EibyeJacobsen, 2004). teleconch and concluded that most of these animals Chancelloriidae complicates (or clarifies) the situ were primitive endogastrically coiled gastropods, ation even more. Sclerites of this group are assembled which he separated into the class Archaeobranchia. in rosettes with one hollow central spine and three or The first members of the more derived gastropod sub more strongly peripheral ones. The microstructure of classes Divasibranchia (Khairkhaniidae) and Dextra these sclerites and general body plan (a hollow, thin branchia (Onychochilidae) (Parkhaev, 2008) simulta walled, elongated sclerite with a distinct basal fora neously appeared in the Early Cambrian. The earliest men) is identical to that of halkieriids and other celo taxa include true bivalves (Vendrasco et al., 2011), the scleritophorans (Butterfeld and Nicholas, 1996; early separation of which within the shelled mollusks Ivantsov et al., 2005; Porter, 2008). They formed is supported by the analysis of the complete mitochon a completely different structure—a hemispherical or drial genome (Plazzi et al., 2013). narrowly conical scleritome with a cavity opening at The microstructure of many shells of extinct and the top (Fig. 4d). Therefore, Chancelloriida were for extant mollusks certainly has certain equivalents a long time considered to be sponges similar to heter among the microstructures of brachiopod shells and actiniids. The lower ends of these organisms were bryozoan skeletons, because they all represent the attached to the substrate, supported by the occur clade Lophotrochozoa (the microstructural similarity rences of complete scleritomes of Chancelloriida in of shells of mollusks, brachiopods, and bryozoans is a the Lagerstätten and reef limestones, where they were good synapomorphy for this clade, which has so far buried in the lifelike position (Zhuravlev, 2001a). rarely been mentioned in papers). In addition, Cam Chancelloriida imprints show a nonporous bilayered brian mollusk shells have crosslaminate, lamello

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 435 fiber, scalelike calcitic and aragonitic and other types a sample of 15 species and together with previous data of microstructures found in mollusks; the difference representing all classes, including newly obtained between the Cambrian and later taxa is that new monoplacophorans, revealed that monoplacophorans microstructures appeared in the course of the mollusk are a sister group of cephalopods within Conchifera, evolution, including the nacre sensu stricto structure whereas scaphopods, gastropods, and bivalves form (Checa et al., 2009; Vendrasco et al., 2010, 2011, a second clade (Smith et al., 2011). Another recent 2013). The appearance of new microstructure types molecular tree, in which Cephalopoda and Aculifera that better resist mechanical stress was caused by an (Aplacophora + Polyplacophora) are sister groups increase in the diversity of predators and their ability to (Vinther et al., 2012), was built by sequencing seven break into the shells (Vermeij, 1990; Wood and nuclear genes in 14 species of mollusks, but it did not Zhuravlev, 2012; Vendrasco et al., 2013). include monoplacophorans. Finally, another molecu The caplike shells do indeed belong mainly to lar tree connecting polyplacophorans and monopla ancient mollusks, i.e., ancestral taxa that gave rise to cophorans (clade Serialia) was built based on the DNA the Later Cambrian–Ordovician radiation of gastro of a monoplacophora specimen; the DNA highly pods, scaphopods, polyplacophorans, and cephalo degraded probably because of bulk fixation of the sed pods (Zhuravlev, 2001). Throughout their evolution iment on the vessel (Giribet et al., 2006). Thus, mor various Bilateria retained the original mineral compo phological, ontogenetic, and paleontological data sition of their shell, which was formed in an equilib support the hypothesis of cephalopod origin from rium with the environment: animals that appeared in motile Early Cambrian mollusks with an external shell the cold “aragonite” eras had aragonite or high mag rather than from some sedentary clonal organisms or nesium shells, and those that acquired a mineral skel softbodied nektonic animals. At least 30 Myr passed eton in warm “calcite” eras have shells with a high between the appearance of the caplike gastropods and magnesiumcalcite composition (Wilkinson, 1979; monoplacophorans and the appearance of cephalo Zhuravlev and Wood, 2008; Porter, 2010). The alter pods, which is sufficient for this evolution. nation of “aragonite” and “calcite” eras depended The occurrence in Herefordshire of Silurian mol mainly on the hydrothermal regime, which influenced lusks (Acaenoplax, Kulindroplax, and others), which the proportions of Ma and Ca ions in the ocean, and combine characters of polyplacophorans (several rows the partial pressure of carbon dioxide, which affected of calcareous dorsal plates) and aplacophorans (man the kinetics of the crystal growth determining their tle groove along the ventral side, or completely shape (the crystalline structures of calcite and arago reduced foot), support the hypothesis of aplacoph nite are different (Sandberg, 1983; Stanley and Har orans having evolved from Cambrian polyplacoph die, 1999; Morse et al., 2006)). orans with calcareous sclerites and a normally devel The shell of the earliest known cephalopod Plec oped foot (Sutton et al., 2001, 2012) (Fig. 1). This sce tronoceras is aragonitic (Landing and Kröger, 2009), nario is repeated in the embryogenesis of although the time of its appearance coincided with the aplacophorans, at least in Caudofoveata (Scheltema “calcite” era. This means that this taxon certainly had and Ivanov, 2002; Nielsen et al., 2007). Early Cambrian ancestors with an external aragonitic While the earliest mollusks, except for Chancellor shell. The most recent studies of Nautilus and coleoids iidae, and annelids were exclusively motile taxa, the showed that they share their ontogentic mode with situation was different among the earliest tentacled gastropods: the embryonic organs form a concentric animals. These mainly include sedentary forms with arrangement around the anteroposterior axis, with a different numbers of valves: from two (as in typical shell plate on the dorsal side (even in shortfin squid brachiopods of all three subphyla: Linguliformea (for with an almost reduced skeleton), whereas the funnel, merly inarticulate brachiopods with a phosphate which is part of the mantle fold, is formed at the pos shell), Craniiformea (inarticulate brachiopods with a terior end of the embryo and turns toward the head calcareous shell), and Rhynchonelliformea (remain with growth. In coleoids the embryonic shell is gradu ing inarticulate and articulate brachiopods with a cal ally shifted within (Shigeno et al., 2008; Kröger et al., careous shell)) up to 30 or more (as in Paterimitra and 2011). Plectronoceras and some of the other earliest Eccentrotheca) belong to the extinct group Tommoti cephalopods retain a number of primitive features in ida discovered in Siberia (Missarzhevsky, 1989). In adults, i.e., the shell was dorsal and the funnel was pos Eccentrotheca, one of the earliest tommotiids, the teriorly positioned, while the paired muscle scars phosphate porous shells (sclerites) were of two types: resemble those in monoplacophorans (Mutvei et al., irregular caplike and flattened. The sclerites were 2007; Kroger et al., 2011). In addition, Plectronoceras arranged spirally and formed a narrow conical external and the majority of the earliest cephalopods lack a skeleton 4mm tall, open at top and bottom (Skovsted protoconch, suggesting that they evolved from benthic et al., 2011). The scleritome of Paterimitra was gener ancestors. Presumably, the protoconch appeared later ally similar to that of Eccentrotheca, but had three and independently in different lineages of cephalo types of sclerites, two of which resembled shells of bra pods that became planktonic (Barskov, 2012). It is not chiopods (Skovsted et al., 2009c) (Fig. 4a). The simi surprising that the most comprehensive molecular larity with brachiopods is emphasized by the identical studies of 1185 mollusk genome regions performed in microstructure with large cavities between the layers of

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 436 ZHURAVLEV shell, microornamentation with a characteristic retic but also included motile epibenthic detritus feeders ulate surface, and the presence of pores with imprints (otherwise, why would they need a protective cover?). of setae (seta are sometimes present due to phosphati It is not certain whether these gave rise to some extant zation), which allows tommotiids to be considered a tentacled Lophotrochozoa or disappeared altogether stem group for brachiopods, whereas the earliest shells like Chancelloriidae, the only known extinct sessile of brachiopods (Aldanotreta, Askepasma, and Salany mollusklike group? golina from the class Paterinata) have a microstructure The discovery of a complete scleritome of halkieri of the tommotiid type (Bengtson, 1970; Holmer et al., ids suggested that these freemoving organisms could 2008b, 2009; Skovsted et al., 2009c, 2011; Topper be ancestral to brachiopods, which became sessile et al., 2013a). The bivalivian tommotiids Micrina and only later and lost all sclerites, except for the two larg Tannuolina, with a few sclerites, are particularly inter est ones that gave rise to the bivalvian shell covering esting as possible transitional forms (Fonin and the dorsal and ventral sides (Nielsen, 1991; Cohen et Smirnova, 1967; Laurie, 1986): Micrina has an embry al., 2003; Malakhov, 2010). However, the most recent onic shell, a bivalvian protegulum with seta sockets. data on the embryogenesis of Novocrania anomala The protegulum in brachiopod embryos is formed (Craniiformea) revealed that its larva lies on the ven before hatching, and one protegulum valve in Micrina tral side during metamorphosis, anchored by the end possesses a crossfolded posterior projection similar to of the posterior larval lobe, which is curved onto the the analogous structure in the Cambrian brachiopod ventral side, whereas the anterior larval lobe forms a Mickwitzia and other Lingulata and suggesting the dorsal mantle lobe and secretes the dorsal valve. The presence of the embryonic pedicle (Balthasar, 2004; development of the ventral valve is delayed, and it is Holmer et al., 2008a, 2011; Balthasar et al., 2009; finally formed by the ventral mantle lobe (Altenburger Skovsted et al., 2009b). et al., 2013). Brachiopods preserved in Lagerstätten Presumably, Linguliformea and Rhynchonelli have their gut preserved, demonstrating that this organ formea could have independently evolved by paedo was Ushaped in different groups (Zhang et al., 2004, morphosis from a bivalvian larva of some tommotiids 2009), and, as is suggested by paleontological evi (Holmer et al., 2011; Skovsted et al., 2011). Moreover, dence, brachiopods could have evolved from sessile different classes of Linguliformea could have evolved tommotiids, which represent the archaic group from different tommotiids: Paterinata, from Eccen Lophotrochozoa. trotheca and Lingulata, from TannuolinaMicrina Sessile tubular tommotiids, like Eccentrotheca, are (Larsson et al., 2014). In general, early brachiopods thought to be ancestral to phoronids (Skovsted et al., show an interesting mosaic pattern: the shells of most 2011). Balthasar and Butterfeld (2009) proposed a dif members of ancient classes, including Chileata, Obo ferent pathway for phoronid evolution, from Cam lellata, Kutorginata, and Paterinata, which became brian brachiopods with a nonmineralized, chitin shell, extinct in the Cambrian or in the early Paleozoic, like Lingulosacculina, through the miniaturization of combine morphological and microstructural charac the organs, which in phoronids are similar to those in teristics of Linguliformea and Rhynchonelliformea brachiopods: dermal muscles and Ushaped gut; lat (Ushatinskaya, 1987, 1998; Popov et al., 1996; Williams eral mesenteries bearing gonads; posterior projection et al., 1996; Malakhovskaya, 2008; Balthasar, 2008; of the coelomic cavity, which was used for anchoring Holmer et al., 2009; Zhang et al., 2011) (Fig. 1). The in the substrate. However, all of these organs are differences between the Cambrian and extant brachi strongly diminished, while setae are absent. Bryozoans opods deepened due to the discovery of a fossil brachi can also be derived from the basic brachiopodlike opod with preserved shell interior, including the pedi body plan as clonal modular descendants of tommoti cle, visceral cavity, and the lophophore. It has become ids that lost the phosphatic skeleton: abundant pri evident that, while the shells of the extant and fossil mary phosphatic taxa existed at the beginning of the Lingulata were superficially similar, their interior was Early Cambrian, when the oceans contained very different, whereas the position of the pedicle and increased quantities of phosphate (Cook and Sher the morphology of the lophophore in many Cambrian gold, 1984). brachiopods have no equivalents among extant brachi However, bryozoans first appeared in the Late opods; for instance, in large, freely lying Heliomedusa, Cambrian and had skeletons of lowmagnesium cal two wide semicircles of dense ciliate setae project cite characteristic of this period (Landing et al., 2010), beyond the shell, as in the larvae of extant Lingula or which could indicate their origin from a softbodied Glottidia (Zhang et al., 2004, 2009, 2011). taxon. Molecular data suggest that brachiopods, Interestingly, two groups of tommotiids, each phoronids, and bryozoans are related within Lopho including one genus (Camenella and Sunnaginia), phorata, which suggests homology of their lopho have dense layers of nonporous paired (mirror sym phores despite some small differences (Nesnidal et al., metrical) sclerites, which were probably arranged on 2013). the surface of the bilaterally symmetrical animals Cotyledion from Chengjiang of China, another rep (Skovsted et al., 2009a; Murdock et al., 2012) resentative of the Early Cambrian Lophotrochozoa (Fig. 4b). This means that the earliest Lophotro with a weakly phosphatized scleritome, has a flexible chozoa were not exclusively sedentary filterfeeders stalk, a calyx, a Ushaped gut with a slitlike mouth,

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 437 and an aboral anus ringed by 30 marginal tentacles. rate micromere 4d, appearing at the stage of 64 cells, This fossil is externally similar to Kamptozoa (Zhang which later evenly divides to form the incipient bilat et al., 2013) (Fig. 1). However, it is significantly larger erally symmetrical mesoderm (annelids, sipunculids, than any extant kamptozoan (5.5 cm instead of 1 cm), echiurids, myzostomids, nemerteans, camptozoans, and the calyx is covered by rounded sclerites. The phoronids, and mollusks; this is lost in brachiopods authors who described this species assume that kamp and bryozoans, but present in acanthocephalans and tozoans could have evolved through miniaturization platyhelminths) and planktotrophic larvae (tro and simplification of the primary organ set in larger chophore) with a prototroch (preoral ciliated band), organisms. The sclerites resemble mobergellans, paired protonephidia, ciliated tuft, and apical plate, phosphate rounded layered shells slightly resembling which is retracted during metamorphosis into the inte larval brachiopod shells. rior, and to form a brain (annelids, sipunculids, echiu Cambrian Lophotrochozoa include another three rids, myzostomids, camptozoans, phoronids, bryozo representatives groups: hyoliths, which survived until ans, cycliophoran, and mollusks; in nemerteans and the Permian in a much more impoverished state than brachiopods there are only cell homologues of the pro in the Cambrian, Early–Middle Cambrian stenothe totroch; the trochophore is considered to have been coids, and Early Cambrian siphonoconchs. Hyoliths lost in cephalopods mollusks and clitellates) (Funch, and stenothecoids, based on the shell microstructure, 1996; Rouse, 1999; Maslakova et al., 2004; Lambert, were more closely related to mollusks (Kouchinsky, 2010; Meyer et al., 2010; Gline et al., 2011; Penner 2000; Feng et al., 2001; Martí Mus and Bergstrom, storfer and Scholz, 2012). Synapomorphies of 2007; Zhuravlev and Wood, 2008), but they consider Lophotrochozoa in the fossil record include the skele ably differed from the latter in the general body plan tal microstructure discussed above and chitinous and were even recognized as the independent phyla (βor γchitin) chetae secreted in saclike invagina Hyolitha and Stenothecata (Runnegar et al., 1975; tions of the cuticle by large epithelial cells (chaeto Sysoev, 1976; Rozov, 1984). The shell in true hyoliths blasts) with microvilli capillaryshaped, traces of was composed of a large conical valve and an opercu which remain (annelids, myzostomids, brachiopods, lum, with two logarithmically coiled supports (helens) polyplacophorans, and juvenile cephalopods, as well sealed with the operculum. In light of the complex sys as bryozoans, in which chitinous teeth in the stomach tem of muscle scars on the operculum, it served not are homologous to chetae) (EibyeJacobsen, 2004; only for the tight closure of the shell by slightly retract Giribet et al., 2009). ing in the conical valve but also for controlling the muscles of the appendages. The combination of the operculum and appendages exclude the presence of a And Many Others muscle foot in hyoliths. They probably just lay on the The Cambrian also yields remains of chaetognaths substrate, supported by the appendages, and could and ctenophores. The latter are buried only in Lager only change position slightly in the direction of the stätten and are very similar to extant species in the bottom currents in order to catch suspended particles general body plan, although some have a different using the mantle trail or a lophophorelike structure, number of combs (Conway Morris and Collins, 1996; which is suggested by occurrences of oriented shells of Chen and Zhou, 1997) (Fig. 1). The most interesting hyoliths in living position on bedding planes (Kruse is the discovery of represented by both et al., 1995). Other hyoliths, Orthothecida, lack Maotianoascus appendages and are commonly found buried vertically. adult and embryonic specimens: this is a radially sym Sometimes adult orthothecids have their gut preserved metrical organism with eight rows of combs lacking due to phosphatization. The gut is composed of tentacles and therefore resembling modern Beroidea straight (anterior) and folded (posterior) regions, as in (Chen et al., 2007). sipunculids; whereas both region of the gut are straight Chaetognaths are very rarely found as complete in hyoliths and juvenile orthothecids (Devaere et al., imprints (Chen and Huang, 2002; Vannier et al., 2007) 2014). Stenothecida were bivalvian organisms that (Fig. 1), but their phosphatized dental apparatus, superficially resemble brachiopods more than bivalves known as protoconodonts (Protohertzina), is com but have serial paired muscle scars as in monopla monly found beginning from the basal Cambrian. cophorans. The third, less well known, group of Cam These remains differ from true conodonts and other brian lophotrochozoan “bivalves” is the class chordates in the microstructure, which are character Siphonoconcha, or Tianzhushanellidae: their symme istic of the skeletal elements secreted on the epithelial try resembles that of brachiopods but with one valve surface rather than in the fold of the epidermis, and with earlike extensions on the area and a valve with a thus they are commonly found as paired aggregates of siphonal groove articulated with dental apparatus several morphologically uniform denticles (Bengtson, (Parkhaev, 1998). All of these groups apparently repre 1983; Szaniawski, 2002). The early appearance of cha sent an early radiation of Lophotrochozoa. etognaths in the fossil record agrees with their position Extant Lophotrochozoa in general retained a few as a sister group of all protostomes in molecular phy synapomorhies. One of the most important synapo logenies (Halanych, 2004) and their unique genome morphies is the spiral determinate cleavage with sepa (Marlétaz et al., 2008).

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It is unlikely that even the best Cambrian Lager organized as in Mandibulata. The nervous system of stätten will produce cycliophores, orthonectids, Alalcomenaeus is more similar to that in Chelicerata, acoelans, or other groups lacking any hard structures. although the anterior pair of limbs on its head region The fossil record of those that colonized land begins in resembles the second pair of appendages of the pecto the midMesozoic by the appearance of the resinpro ral segment in Stomatopoda. ducing gymnosperms (in amber). Scientists some Despite all their peculiar characteristics, Ediacaran times (with much success) attempt to infer the pres and Early Cambrian organisms cannot be considered ence of these organisms from characteristic injuries in “helpless monstra,” not even as variations of “archaic the skeletons of trilobites, crinoids, and other inhabit diversity” but as a world of organisms adapted to par ants of ancient seas, but only in those tha became par ticular environment that essentially changed during asites. However, there are several “unidentified the Cambrian: from seas with low oxygen content in objects,” including calcareous spirally coiled shells of the bottom water layers to well aerated waters filtered cribricyaths, conical shells of Solterella with alternat by the pellet conveyor belt; from a cold to warm cli ing agglutinated and secreted layers, imprints of mate; from almost virgin, favorable substrates to medusoid parapsonemids with a Ushaped gut and almost motionless and weakly attached filter feeders to tentacles encircling the mouth, and some remains strongly bioturbated sediment (substrate revolution); from the Burgess Shales and other Lagerstätten that from several slow predators to a vast diversity of active cannot be currently placed (Amiskwia, Dinomischus, benthic and nektonic chasers. For instance, the Cam Odontogriphus, and Oesia) (but these are unlikely to brian “explosion” was followed by the “Great Ordovi include acoelans or acanthocephalans). cian Revolution.” The world of Metazoan organisms Previous discussion shows that Cambrian fossils, renewed four times in the geologically short interval of including sponges, cnidarians, cephalorhynchs or 80 Myr from the midEdiacaran to the beginning of annelids, arthropods, mollusks, brachiopods, echino the Ordovician: Late Ediacaran, Early Cambrian, derms, or chordates, let alone tommotiids or chancel Middle Late Cambrian, and Paleozoic (formed in the loriids, lack key characteristics occurring in the extant Ordovician) biotas differed from one another more members of these clades, and commonly even in their than the Paleozoic biota differed from the MesoCen nearest (Ordovician) descendants. All of these fossils ozoic, which existed for approximately 250 Ma each. represent ancestral groups or their extinct branches. For instance, new microscopy methods showed that, among Cambrian arthropods, which less than 10 years CONCLUSIONS: THE LONG OVERTURE ago were thought to be good examples of terminal OF THE CAMBRIAN “EXPLOSION” groups of crustaceans, i.e., Branchiopoda and Phyl Many hypotheses about the origin of life on Earth lopoda (Isoxys, Canadaspis, Rehbachiella), and ostra are faulty in that the evolutionary events are not linked codes (bradoriids, phosphatocopids), include no to the actual environment and everything in these the taxon with a set of limbs that would allow its unequiv ories happens in a kind of void. Some publications on ocal assignment to a class of crustaceans or could be the Cambrian period suggest that the skeleton of identified with certainty as Mandibulata. They can Ecdysozoa was formed in animals inhabiting the lit have giant grasping appendages instead of antennae or toral, partly submerged in water, whereas coastal areas a hypostome connected to the anterior pair of append were covered by sand because of the washout from the ages. Epipodites specialized for breathing or osmoreg empty, forestless land. In fact, all of the first Ecdysozoa ulation can be completely absent, whereas all head and other animals lived in a normal marine sublittoral appendages can be totally uniform, indistinguishable environment (Burzin et al., 2001, textfigs. 10.3, from the walking limbs, etc. (Stein et al., 2008; Maas 10.4), and the mineral skeleton in different groups, et al., 2009; Vannier et al., 2009; Haug et al., 2010, even within the Ecdysozoa, formed independently, at 2012; Legg et al., 2012, 2013). different time and in each group, completely reflecting Very interesting data on the organization of the ner the chemical composition of oceanic water of the cur vous system on the earliest arthropods were obtained rent epoch (Zhuravlev and Wood, 2008; Maloof et al., by studying the most common Chengjiang fossils 2010a; Kouchinsky et al., 2012). The expansion of (Fuxianhuia and Alalcomenaeus): a combined use of animals first to the littoral and then onto the land Xray computer tomography and fluorescent micros began from the sublittoral (Mangano et al., 2014). copy shows the distribution of iron and other chemical Thick, sandy series began accumulating by the end of elements in clay minerals replacing the soft tissues, the Devonian Period with the appearance of forests thereby showing a very fine detail of the nervous sys and mycorrhiza, a very strong destructive factor for tem up to the optical nerve and nervous fibers leading rocks (Bonneville et al., 2009; Davies and Gibling, from various parts of the brain to the limbs (Ma et al., 2010). 2012; Tanaka et al., 2013). It was demonstrated that To some extent, with little connection to actual Fuxianhuia, which has been treated in all phylogenetic time and space, Nielsen (2012, 2013, p. 171), pro trees as a basal Chelicerata (Chen et al., 1995b; Wills, posed a hypothesis of primary ciliated holopelagic 1995; Legg et al., 2012, 2013), had a nervous system organisms rooted in Haeckel’s “Gastrae” theory, say

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 439 ing that “Information from the fossil record …and cribriciates—30; corallomorphs—32; stenothe from genetics gives no direct information about the coids—16; brachiopods—233; hypoliths—78; orth ancestral eumetazoan life cycle.” According to this thecans—77; sabeliditids–lyditids—6; hyolithelm “superimposition model,” the holopelagic gastraea inthes, tommotiids, and other primitive sessile was the ancestor of the eumetazoans with the indepen Lophotrochozoa—105; echinoderms—76, grapto dent addition of benthic adult stages in various clades. lites and pterobranchs—48) (Zhuravlev, 2001). If the The opposing intercalation theory proposes a benthic events are considered stage by stage, the proportion of gastraea with planktotrophic larvae evolving indepen sessile and slightly moving taxa was approximately dently in numerous lineages through ontogenetic 50% in the first half of the Cambrian, and by the mid intercalations. dle of this period it had decreased to 20%, whereas the Nielsen based his theory on a comparative analysis proportion of the motile nektonic forms in the same of the embryology and morphology of extant represen interval increased from 5 to 20% (Wood and Zhurav tatives of various phyla of Eumetazoa (Cretaceous lev, 2012). Similar figures were obtained by compara echinoids, which he used as an illustration, is also a tive analysis of biovolumes of the Early and Middle modern group, unrelated to the primary evolution of Cambrian communities: the number of individuals of Eumetazoa and even echinoderms) and from the species (both planktonic and nektonic lifestyles) assumption that the independent, numerous appear (Conway Morris, 1986; Ivantsov et al., 2005; Caron ances of a planktotrophic larva could not be adapta and Jackson, 2006; Dornbos and Chen, 2008; Zhao tionbased. It appears that this assumption is not cor et al., 2013). rect, because the ancient organisms are far from being Second, the Early Cambrian epoch shows an identical to their extant relatives morphologically and unusual high provincialism of marine fauns, which did in lifestyle, and probably in embryogenesis. For not have any equivalents in the whole of the Phanero instance, the protoconch in Cambrian mollusks and zoic history of Earth, even at the times of the largest some other Lophotrochozoa was larger than in later regressions leading to the development of numerous taxa with a planktotrophic larva and thus indicates isolated basins. The indicators of β diversity (the dif their benthic affinity (Nützel et al., 2007; Runnegar, ference of the specific and generic composition of the 2007). Brachiopods with a larval shell, which could be adjacent paleocommunities) reached the same values planktonic, appear in the middle and at the end of the as the indicators of the γ diversity (the difference in the Cambrian (Popov et al., 2012). generic composition between the adjacent paleoprov Thus, the fossil record presents several indepen inces; the species composition was not entirely the dent lines of evidence of planktotrophic larva being a same (Zhuravlev and Naimark, 2005)). The same was late acquisition in Metazoans, even in the presence of observed in the Ediacaran period, although it is many fossil embryos with direct development in the described today only at the qualitative level, i.e., there absence both planktotrophic and lecitotrophic larvae is a strict connection of certain paleocommunities to (Donoghue et al., 2006). Direct evolution is observed regional facies complexes (Grazhdankin, 2004; not only in embryos of Cambrian Ecdysozoa but also Lafamme et al., 2013). An exceptionally high level of in synchronous embryos of cnidarians and cteno provincialism is also observed among ichnofossils, phores (Kouchinsky et al., 1999; Dong et al., 2013). although nothing seemingly should have obstructed In addition, the planktonic and nektonic commu the parallel development of similar behavior forms in nities with many metazoan animals were formed only different groups, as in all later epochs (Jensen et al., in the late Cambrian–Ordovician, which is supported 2013). This situation was unlikely to be possible, if the by the morphological analysis of the body plan of Early Cambrian organisms had a planktonic stage in actual groups, and such important and independent their ontogeny. pieces of evidence indicate the time of the beginning As for the reasons leading to the appearance of of the fecal pellet production, i.e., the time of the for a planktotrophic larva, the most important was the mation of the planktonic community (Signor and Ver substrate revolution, the development of which we can meij, 1994; Logan et al., 1995; Rigby and Milsom, observe from ichnofossils, a separate group of paleon 2000; Butterfeld, 2001; Zhuravlev, 2001b; Vannier et tological objects. In many cases traces are difficult to al., 2007; Ponomarenko, 2008). On the whole, of the link to organisms, but their examination facilitates an 4367 genera of Cambrian fossils, 77% are motionless understanding of general trends in the evolution of benthos (mollusks—308; halkieriids and others, behavior and in some cases point to the first appear primitive motile Lophotrochozoa—180; trilobites— ance of some groups. It was previously thought that the 2408; bradodoriidae and phosphatocopids—168; first bilaterally symmetrical traces certainly indicated arthropods with nonpmineralized skeleton—118; the presence of Bilateria. However, such tracks can be ctenophores, cephalorhynchs and annelids, xenu also left by marine protists, like Rhizaria (Matz et al., sians, anomalocaridids, parapsonemids remichor 2008). In any event, tracks that can be linked to any dates and chordates—102; conodontophorides and activities of Bilateria, e.g., simple sinusoidal Helm chaetognaths 3) and 23% are attached or slightly mov inthoidichnites, appeared only by the end of the Edi ing benthos (archaeocyaths and radiocyaths—309, acaran, later than vendobionts. An explosive diversifi

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 440 ZHURAVLEV cation of traces of Bilateria began in the Cambrian, Hejnol, 2009), and the genes necessary for that, are parallel to the diversification of skeletal organisms, retained in sponges (Conaco et al., 2012; Kerner et al., and resulted in the formation of a welldeveloped, 2013), given the resemblance of the expression of the multitiered, and diverse infaunal community complex of regulatory genes connected with the for (Fedonkin, 1985; Droser and Li, 2001; Crimes, 2001; mation of the blastopore, mouth and anal openings in Gámez Vintaned and Liñán, 2007). All of these events Ecdysozoa (priapulids, some arthropods), Lophotro happened in a normal marine sublittoral zone, from chozoa (some mollusks, annelids, and nemerteans), which bioturbators had spread to the shallow water up and Deuterostomia, the structure of which is deter to the periodically exposed littoral and toward the mined by the original body plan for all Bilateria (Mar continental slope only by the midCambrian. A sud tinDuran et al., 2012). Moreover, ancestors of Bilate den increase in the rate and level of bioturbation, i.e., ria, probably had serial paired appendages (Pangani by six times by the end of the Cambrian, resulted in a ban et al., 1997; Shubin et al., 1997; Jacobs et al., profound impoverishment of the fauna of sessile and 2007; Prpic, 2008) that were most likely similar to cni sedentary organisms; some of each, e.g., cnidarians, darian tentacles or the smooth appendages of some managed to colonize the pelagial (Wood and Zhurav xenusians. lev, 2012; Mangano and Buatou, 2014). This process is Indeed, the remains of sessile skeletal Lophotro referred to as the substrate or agronomic revolution chozoa, which could be ancestors of brachiopods and (Seilacher and Pfüger, 1994; Bottjer et al., 2000). The other tentacle animals (tommotiids), appear in the intensive, constant reworking of the substrate pre fossil record later than remains of motile Lophotro cluded larvae from surviving on the surface of the sub chozoa (mollusks and halkieriids) (Zhuravlev and strate, whereas new communities in which the larvae Wood, 2008; Maloof et al., 2010a; Kouchinsky et al., could attach and survive, e.g., hardgrounds and rock 2012). Even modern brachiopods retain some charac grounds, had not yet formed (Vermeij, 1990; Zhurav ters of metamery, i.e., three body segments (Malakhov lev and Wood, 2008). and Kuzmina, 2006), like phoronids, in which two The effect of transcription factors and the expres such segments can be recognized (Temereva and sion of various complexes of regulatory genes in the Malakhov, 2006). Among Ecdysozoa, the oldest larval evolution of mollusks, echinoderms, and some known group is Xenusia with serial appendages, which other groups indicate the independent and repeated have the original body plan in cephalorhynchs, on one emergence of a planktotrophic larva and its most hand, and in tardigrades, onychophorans, and arthro important organs (apical plate, prototrach/neotrochs) pods, on the other (Gamez Vintaned et al., 2011; in different groups of Bilateria (Sly et al., 2003; Dunn Caron et al., 2013b). The fossil record of chordate and et al., 2007; Raff, 2008; Nakano et al., 2013). Even echinoderms begins with bilaterally symmetrical very similar larvae of chordates and Ambulacralia organisms, which have serial organization of some appeared independently, based on the sequence of organs, e.g., the gill apparatus (Shu et al., 2003b; gene expression (Lacalli, 2005; Swalla and Smith, Zamora et al., 2013). 2008). Taking into account the data on the evolution of the In contrast, the total data on comparative mor complex of regulatory genes (Schierwater and phology and embryology and molecular phylogenetic DeSalle, 2001), germline cells (Buss, 1987; Black analysis, including a comparison of the complete stone and Jasker, 2003; Extavour, 2007), and larval genomes and sequence of expression of the genes of development (Blackstone, 2009), we can suggest the the Hox complex, suggests that the stem group for independent evolution of bilaterally symmetrical and Bilateria were not just bilaterally symmetrical animals other multicellular animals, which was accompanied but triblastic animals (with muscle cells of mesoder by the parallel development of a number of structures mal origin), apparently serial, with a distinct antero in both groups. These factors apparently explain their posterior and dorsoventral polarity and with an accu almost simultaneous appearance in the fossil record mulation of nervous cells in the head region (Bala and the parallel explosive diversification of sponges, voine and Adoutte, 2003; Prud’homme et al., 2003; cnidarians, ctenophores, and Bilateria as skeletal and Malakhov, 2004, 2010; Finnerty et al., 2004; Boero softbodied, as well as traces. et al., 2007; Gabriel and Goldstein, 2007; Arendt Could the Cambrian “explosion” truly happen, or et al., 2008; Prpic, 2008; Williams et al., 2012; Chese it is only an epiphenomenon predetermined by bro et al., 2013; Janssen and Budd, 2013). For changes in the sedimentary settings at the Crypto instance, ctenophores have several types of mesoder zoic–Phanerozoic boundary? The “explosion,” as mal cells (muscular, mesenchymal, and others) and mentioned above was not instantaneous; it was longer branched off the rest of Metazoa before branching of than seconds or even a few million years. From the Cnidaria and Bilateria. Assuming that the mesoderm appearance of the first skeletal Metazoa (Namaca of Ctenophora is indeed homologous to that of Bilate lathus) and those possibly belonging to Bilateria 555 Ma ria, the early development of the mesoderm in meta to the formation of the entire Metazoan assemblage zoan animals, with its subsequent loss in Cnidaria, (even if we do not omit bryozoans and groups absent in Placozoa and possibly Porifera (Martindale and the fossil record (echinoderms were the last to appear

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 THE EARLY HISTORY OF THE METAZOA 441 as skeletons, ca. 515 Ma)), the duration of that calcu and polarization of epithelial cells, the synthesis of lated explosion is 40 Ma, which is quite a long time. which is increased during the formation of fruiting However simple the Ediacaran and Early Cambrian bodies, resulting in the formation of a polarized epi Metazoa might have looked, these were relatively well thelium in Dictyostelia (Dickinson et al., 2011). It is developed animals with a complete genetic apparatus, important that slime molds have migrating pseudo the assemblage of which needed a long time. If we can plasmodia, or aggregates of amoeboid cells, and can not find clear precursors of these organisms, perhaps cross soil barriers impermeable for solitary cells the genetic apparatus could have evolved separately (KuzdalFick et al., 2007). This is an adequate reason from them? for the evolution toward multicellurity. Thus, aggrega Indeed, the complex of the key Metazoan partici tional, multicellular organization occurs among the pating in the embryogenesis, sexual reproduction, and lower Opisthokonta: amoeba Capsaspora, assigned to apoptosis, i.e., the controlling factors regulating tran Filasterea, sister group, of Choanofagellata + Meta scription (Brachyury, RUNX), adhesion, and polar zoa, and cellular slime mold Fonticula from Nuclear ization of cells in tissues (genes synthesizing catenines, iidae, sister group of Fungi (Brown et al., 2009; Sebé laminines, cadherines and integrines), communica Pedrós et al., 2013). tive intercellular systems (ancestral Notchtranscip The eukaryote fossil record, which does not take tion complex), cell differentiation (genes synthesizing into consideration various “plant” remains (Virid tyrosinases), and genes producing neuromediators iplantae, Stramenopiles), contains traces in the beds (neuropeptides) present in Choanofagellata, Ichthy 1.70–0.55 Ga similar to Horodyskia (they were origi osporea (Creolimax, Sphaeroforma), Filasterea (Cap nally identified as hydroid colonies connected by saspora, Ministeria), Chytridiomycota, the basal group thalli) (Fedonkin and Yochelson, 2002)], Myxomi of fungi, and Apusozoa (Amastigomas), and in fungi todes, and Gaojiashania (Fig. 1, Amoebozoa). They and choanoflagellates, part of this gene complex (from differ from traces of bilaterally symmetrical animals in 30 to 50%) could have been secondarily lost (Nichols several characteristics: they are chaotic (traces of Bila et al., 2010; SebePedros et al., 2010; Fairclough et al., teria have a regular pattern; Fedonkin, 1985), form 2013; Suga et al., 2013; Suga and RuizTrillo, 2013) loops, bifurcate, vary in width within the same trace, (Fig. 1). This gene complex is turned on the stage of and can become chains of globular structure (Bengt the formation of colonies and controls the synchroni son et al., 2007; Zhuravlev et al., 2009; Gámez Vin zation of cell division, and it is also used in the mitosis taned and Zhuravlev, 2013). The mineralogical and and production of protein necessary for building a elementary composition of the globular structure and tubulin cytoskeleton, which is facilitated by alternative traces are also identical (Meyer et al., 2012). Such splicing and enables the synthesis of different proteins traces are in laboratory experiments are left by migrat on the basis of the same gene, which determines the ing pseudoplasmodia Dictyostelia, which at the end of growth of protein diversity and expands the complex the life cycle form fruiting bodies as a globular head of ity of gene regulation (SebéPedrós et al., 2013). spores covered by a hard cover and attached by a stalk Except for Apusozoa, all of these organisms belong to (Wallraff, E. and Wallraff, H.G., 1997; Sternfeld and singlecelled organisms capable of forming colonies of O’Mara, 2005; Bonner, 2006). Another branch of Opisthokonta, which are basal for the Metazoa Amoebozoa (Lobozoa) exists at least 0.8–0.7 Ga and (Chytridiomycota), whereas Apusozoa is probably a is represented in the fossil record by the shells Melano sistergroup of Opisthokonta and is the transitional cyrillium and similar forms (Porter, 2006). group between these organisms and Amoebozoa. Fungi that can be recognized from hyphae with or The latter group, based on the molecular data and without septa, or by the presence on the same substrate structure of organelles, is considered the sister group of organisms characteristic for the lifecycle of fungi, of Opisthokonta, and both are assigned to Unikonta are known from approximately 1.0 Ga in the fossil (Baldauf, 2008; Eme et al., 2011; Torruella et al., record (Burzin, 1993; Javaux and Marshal, 2006; Por 2012). ter, 2006; Nagovitsyn, 2008; Butterfeld, 2009; Ger The gene complex of Metazoa apparently began man and Podkovyrov, 2010) (Fig. 1). The former forming before the appearance of Opisthokonta: in belong to Ascomycota and the second belong to the Dictyostelia (previously assigned to the class Acrasio Chytridiomycota, although it is difficult to assign them mycetes in the section Myxomycota), the best studied to extant groups. group of Amoebozoa, shows diverse signal Metazoan The first vendobionts appeared 0.58 Ga, represent molecules, including transductors, attractors, and ing a transitional stage between the multicellular fungi activators, causing aggregation and differentiation of and animals belonging to Opisthokonta: a rigid con the cell, which could include up to five different types struction with a fractal system of canals suitable for (Saran et al., 2002; Eichinger et al., 2005; Schaap, osmotrophy above the substrate surface and inside the 2007), homeobox genes (Wariai), which are responsi substrate (Fig. 1, Vendobionta). Apparently, by the end ble for the development of the anteroposterior axis of the Ediacaran (not later than 0.55 Ga), the Meta (Han and Firtel, 1998), and proteins relative to α and zoan gene complex in the ancestors of multicellular βcatenins that playing a leading role in the adhesion animals had been completely formed, which predeter

BIOLOGY BULLETIN REVIEWS Vol. 5 No. 5 2015 442 ZHURAVLEV mined the Cambrian diversification. Therefore, we see genesis and therefore are not homologous to choano here the almost synchronous appearance of primitive cytes in Choanoflagellata (Maldonado, 2004; Carr members of Ecdysozoa (xenusians, anomalocaridids, et al., 2008; Fairclough et al., 2010, 2013; SebéPedrés early cephalorhynchs and arthropods, later tardi et al., 2010; Suga et al., 2013). grades, pycnogonids, and pentastomids), Lophotro chozoa (tommotiids, halkieriids and other celoscleri Thus, the hypothesis of a planktonic filter–feeding tophores, hyoliths, stenothecoids, siphonocochs, ancestry needs to be refuted and a different scenario ancient mollusks, brachiopods, annelids, and possibly put forward, i.e., on the surface of the substrate inhab kamptozoans, and later—bryozoans), Deuterostomia ited by slime molds. Traces of organisms similar to (early groups of echinoderms, hemichordates, and slime molds are found on substrate surfaces dated chordates), Ctenophora, Calcarea and Silicea 1.70–0.55 Ga. Moreover, the only distinct evidence of (archaeocyaths, heteractinids, and others), Cnidaria the presence of the Metazoa and even the Bilateria in (corallomorphes, hexaconylariids, hyolithelminthes, the PreCambrian, at the very end of the Ediacaran and later—conulariids and medusoids), and Chaetog (<0.55 Ga), are marine trace fossils, including hori natha (protoconodonts), as well as an explosive growth zontal tunnels, surface tracks/trails, and vertical traces of their diversity (Fig. 1). (Gámez Vintaned andLiñán, 2007; Chen et al., 2013). This sequence of events does not agree well with The surface tracks are particularly interesting, because molecular clock data. However, the precision of the the two series of parallel pits or scratch marks have a molecular clock is strongly influenced by unequal evo bedding surface undisturbed between them (no trail lutionary rates within different groups, the selected left by a body in between), indicating that they were statistical methods for primary data processing, and probably left by an organism with appendages. To many other assumptions of molecular biology, as well “make” a multicellular organism out of a conventional as system biases (Ayala et al., 1998; Bromham, 2003). slime mode organism (an amoeboid aggregate capable Therefore, drastically different molecular histories of of movement), it is sufficient for the mechanisms that the Bilateria exist—from long and cryptic ones that turn on at the stage of the fruiting body formation (cell are not reflected in the fossil record to those that are differentiation, the epithelium formation, and the close enough to an observed sequence of the first gamete germination) to became operational at the appearances of diverse groups of organisms in the fos stage of the feeding motile stage of a slime mold with sil record advocated above (ArisBrosou, Yang, 2003; gametes. Such a confluence of two life stages would Peterson et al., 2004; Cartwright, Collins, 2007; simultaneously provide an opportunity for metazoan Chernikova et al., 2011; RotaStabelli et al., 2013). genes to be coopted from the genes and to be based on A compromise between the fossil record and a regulating mechanism that previously functioned in a sequence of events suggested with the point of cell aggregations. In the unicellular Opisthokonta and a pipette is commonly searched for in those hypothet Dictyostelia, such regulatory mechanisms begin oper ical ancestors of the Metazoa that could not be fossil ating during colony formation. The extant basal ized, e.g., Haeckel’s Gastraea. Opisthokonta are characterized mostly by clonal and syncytial colonies, but the genetic toolkit responsible A Gastraealike metazoan progenitor would be for cell adhesion and polarization and a cascade of improbable, since the planktotrophic larva was a late gene modifications, followed by multicellularity, is development in the Metazoa, large planktonic and deployed in aggregative amoeboid colonies (Sebé nektonic organisms did not exist at the beginning of Pedrés et al., 2013). the Cambrian, and all Cambrian fossil embryos belonged to direct developers. It is noteworthy that the Vendobionta show evi More attractive is Zakhvatkin’s (1949) hypothesis dence of a life cycle similar to that of slime molds. Ven of a synzoospore, which was developed recently by dobiont fossils from the Trepassy Formation of south Mikhailov et al. (2009, p. 764). It suggests that a mul eastern Newfoundland can be arranged in a succession ticellular animal appeared as the result of “…the evo of organisms (possibly a life cycle) consisting of organ lutionary transition from temporal cell differentiation isms different in size and lifestyle but possessing the to spatial cell differentiation,” i.e., by the integration same type of frondlets. The succession includes a fusi of several cell types existing at different successive form freelying or even slightly motile Fractofusus—a ancestor’s life cycle stages into a single multicellular sedentary bushlike frondose Bradgatia—and a small filterfeeding organism, which gave birth to all the sedentary stalked frondose Charnia masoni growing other Metazoa. into a big one (up to 1 m high) Charnia grandis with a However, in some specialized planktonic filter welldeveloped attachment disc (Brasier and Antc feeders, e.g., Choanoflagellata, which are proposed as liffe, 2004) (Fig. 1, Vendobionta). These could indeed a hypothetical metazoan progenitor, a number of represent an extinct intermediate group of the multi important gene complexes have been apparently lost, cellular Opisthokonta, being neither fungus nor meta whereas colony formation is carried out through cell zoan. Assuming that Metazoa are possible descen divisions that are not synchronized, and sponge cho dants of organisms resembling migrating slime molds, anocytes arise from noncollared cells during embryo the Fungi could be descendants of its fruiting stage.

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After all, we are all Unikonta and need to have a com ArisBrosou, S. and Yang, Z., Bayesian models of episodic mon ancestor. evolution support a Late Precambrian explosive diversi fication of the Metazoa, Mol. Biol. Evol., 2003, vol. 20, no. 12, pp. 1947–1954. ACKNOWLEDGEMENTS Ayala, F.J., Rzhetsky, A., and Ayala, F.J., Origin of the I am extremely grateful to the reviewers for their metazoan phyla: Molecular clocks confirm palaeonto critical review of the paper and for their useful com logical estimates, Proc. Natl. Acad. Sci. U.S.A., 1998, ments and to the artist Vsevolod Abramov for making vol. 95, no. 2, pp. 606–611. reconstructions based on the author’s ideas. This work Babcock, L.E. and Ciampaglio, C.N., Frondose fossil from is supported by my own enthusiasm and the compas the Conasauga Formation (Cambrian: Drumian Stage) sionate attitude of “National Geographic Russia.” of Georgia, USA, Mem. Assoc. Aust. Palaeontol., 2007, vol. 34, pp. 555–562. 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