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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
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



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



1700 1000 580 550 540 million years
Xenisia Arthropoda
Vetulicolia Priapulida
Palaeoscolecida Nematoda
Coeloscleritophora Nemertea
Amoebozoa Phoronida
Tommotiida Platyhelminthes
Vendobionta Rotifera



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
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


Liu et al. 2007). 5 2015 . 1999. molluskan “bod cleavage to gastrulation and the development of the ies” are preserved in extreme circumstances. Steiner et al. Smith and Caron (2010). contain only small phosphatized 2014.. although the Ecdysozoa The Örstentype Lagerstätten.. THE EARLY HISTORY OF THE METAZOA 419 j h g i c e f d b a Fig. species instances. where phores. 1979. which should Ecdysozoa is the overall dominant group (Zhao et al. 2012). 2004. belong to Ecdysozoa (Müller. and some inserta sedis groups. Kouchinsky et al. Chen et al. they were preserved as calcite infills within nodules such as Pseudooides. with the same total result: al. (2011). The ani mal reconstructions are modified after Budd (1998). are sometimes assigned to cteno the Silurian Herefordshire Lagerstät (425 Ma). whereas Lophotrochozoa are entombed in an ancient volcanic ash (Sutton et al.. 2001. named after the affinity of some embryos of “Cnidaria” or “Cteno type Late Cambrian locality in Sweden. (2014). be arranged in successions from the initial stages of 2013).. (2007).g. larvae. (2011). all of which except in extremely rare estimate other ecological parameters. (i) Hurdia. Aldridge et al. 2009). 2014). e. 2.. Maas et diversity or abundance. the Burgesstype. in contrast to phora” cannot be completely excluded (Liu et al. (2011b). absent (Bengtson and Yue. 5 No.. in adult organism.. (d) Diania. and fragments of tentacles (Zhang et al. cnidarians. Gamez Vintaned et al. In other types of occurrences. 2006). Daley et al. (c) Microdictyon. The phosphatized embryos.. Hou et al. (2009). It is possible to large organisms. (g–j) Anomalocaridida: (g) Amplectobelua. and lophophore with ciliated remains. (b–f) Xenusia: (b) Mureropodia..g. (j) Vetulicola. Cambrian Ecdysozoa: (a) paleoscolecid worm. e. Zhuravlev et al. (2011). digestive tract. pedicle. Ou et al. 1997. (h) Nectocaris. (1999). Ma et al. (e) Anten nacanthopodia. BIOLOGY BULLETIN REVIEWS Vol. © Artist Vsevolod Abramov. (f) Pambdelurion. including embryos..

5 2015 .420 ZHURAVLEV 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.. entitled (with reason) “A Merciful integuments but also to the geochemistry of the Edi Death for the ‘Earliest Bilaterian.. conclusions recently published in teria (Bailey et al... However.. more than 160 citations... Vanreusel et al. These eralogical study of these microfossils and their chemi publications address the occurrence in the Cambrian cal element composition (C. Min Smith (2013). From the view gren et al. 2007).’ Vernanimalcula” acaran–Cambrian oceans. as reconstructed by gastrulae (Cunningham et al. in which they calculated that the fact. (2004a) has attracted even in simple embryos in the early stages of splitting.. 2009. which still retained fea concluded. 1990. 2008). Ca. These fields serve ance is observed in cysts of Holozoa (Protista) (Huldt as the basis for modern paleontology. Imaging Smith and Caron (2010) and Smith (2013). Viridiplantae. Viridiplantae and Rhizaria that were common in the This taphonomic background was necessary. The In gastrulae such a row precedes the development of bestknown Ediacaran Lagerstät of this type is a Dous the gust. Thus. in Guizhou. very regular dichotomous the deepest water Cambrian assemblages (sublittoral) branching and arrangement of tabulae. P. 2004). the circulatory system. The probable existence of such these structures as colonial bacteria or embryos such as an ancient cephalopod. The socalled spiculate sponges from (Li et al. Among nature: neither the microstructure. gut. 1998). 2011). are renalcids—organisms of uncer tations to life in an oxygendepleted environment tain affinity resembling some algae from the groups (Ivantsov et al.. 2014). based on the study of fibronormal crystals tures of the stratified Canfield Ocean (Canfield. It must China. 2014). and a funnel (hyponome) suitable for BIOLOGY BULLETIN REVIEWS Vol. while priapulids sponge spicules (Yin et al. etc. 2013.. 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. Yin et al.. (2012). they were mainly formed in late diagen was previously interpreted as belonging to Arthropoda esis. and giant sulfur bac point of taphonomy. 2010. among the millions of phosphatized (630–620 Ma). paired coelomes. 1998). that the dominance of Ecdysozoa in all these assem eyes.. (Li et al. presumed embryos. However. Such an analysis is pret. including publications on the As for the Cambrian Lagerstätten. nor chemical com Loricifera. and even cancer.. U. 2012a. which. Gill et al. 2010). 2001). well synchrotron radiation microtomography of some developed gills. 1998. 5 No. organic matter of uncertain origin possessing micro 13C/12C) and the increased content of Mo. had paired techniques using propagation phasecontrast based cameralike eyes on short stalks. Analysis of (diameter less than 100 μm)... system. 2h). EdiacaranCambrian (Liu et al. 2010). Bengtson et al. their role in the paleocommunities are largely judged Phosphatized embryos were also difficult to inter from the analysis of Lagerstätten. and even layers of diagenetic prestigious journals by Smith and Caron (2010) and phosphate mineral (Bengtson and Budd. 2005). in Vernanimalcula. 2012b). see Butterfeld. 2013). Some the Weng’an phosphorite are likewise of inorganic Ecdysozoa are adapted to such conditions. mineralogical. microfossils. 2010. This locality contains giant acritarchs. whereas micromeres give rise to integument hantuo phosphorite Lagerstätte. corals.. and the complexity can be found. sponges. 2006. the paper by Bengt blages is related not only to good preservation of their son et al. as well as the shows that they included species with different adap lack of partitions. 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. and V scopic cracks.” activity (Donoghue et al.. 2011a). the Doushantuo phosporites suggest so far that multi Chen et al.” in light of their microscopic size (Oeschger.. thereby excluding the possibility of interpreting or Chordata) (Fig. Pi et al. and isotope analysis (34S/32S. 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. The structures inter and nematodes can live through long periods of anoxia preted as “corals.. multiple objects with similar shape or algae. which was concluded based on sedimentologi of diagenetic (secondary abiogenic) modification of cal. 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). seem insufficiently substantiated. Liu et al. 2009)—possibly original article by Chen et al. 2011. like finding a pebble strik earliest Bilateria (Vernanimalcula) with a circulatory ingly similar to a chicken bone on a large beach. nearer the “ventral side. in the thick phosphotite Weng’an member be noted that. 2004. Zhuravlev because the appearance of the ancient organisms and et al. it should be said origin of bilateral symmetry. appeared earlier. South cells (Chen et al. the same appear tion of dead organisms into fossils). cellular algae (Viridiplantae or Stramenopiles) existed (2012) published a particularly high impact paper on at the beginning of the Ediacaran period (which. Yin et al. lateral fins. of the apatite minerals forming this fossil..

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

3c. Ediacaran Vendobionta: (a) Tribrachidium (Triradialomorpha). which is impossible even Proarticulata (Fig. (2008). 2002. (f) Dickinsonia (Proarticulata). 2003. It is this system of units that rigid organic film present in the fungi and algae found gives vendobionts their quiltlike appearance (Xiao et BIOLOGY BULLETIN REVIEWS Vol. Seilacher (2002). and 3j). details of their morphology. Naimark and Ivantsov. in the presence of a system cliffe and Brasier. vendobionts. growth with terminal. Brasier et al. Brasier and Antcliffe (2008). the more prominent is the morphology of pha (Figs. they have on their surface a ning and digital mapping. including bipolar.. 2008). 3e). Grazhdankin. gut. in the same beds (Grazhdankin and Seilacher. 2008. (c) Fractofusus (Rangeomorpha). the largest difference is in the internal dankin and Seilacher. 3f). Bilateralomorpha) or thin for organisms with a mineral skeleton. Ant structure of the organisms. asymmetric Grazhdankin. not isometric.422 ZHURAVLEV j b d g f c h a e i Fig. The coarser the bifurcating canals arranged in one plane (Rangeomor sediment is.. Droser et al. without losing (the length of the chambers greater than the width by one–two orders of magnitude) (Petalonamae (Fig. (g) Paravendia (Proarticulata). Zhu et al. (e) Pteridinium (Petalonamae). Arboreomorpha (Fig. (2012). © Artist Vsevolod Abramov. 2004. Zhu et al. The reconstructions are modified after (2004). When the same species are buried in a which was revealed using high resolution laser scan finegrained sediment. 3. (i) Nilpenia. of tubelike units chambers (vanes) that are subquad In addition. (2014). Serezhnikova (2007). 5 2015 . 5 No. 3b. 3d)). 1993a. 2002. any kind of zooids and unlimited. 2009). Peterson et al. vendobionts are often preserved in large rate in a crosssection and penetrating the entire body numbers in coarsegrained sandstones. (d) Charniodiscus (Arboreomorpha). insertion of new frondlets (Zhuravlev. (h) Eoandromeda. Grazh However. j) Beothukis (Rangeomorpha). (b.

resulting in a 1994. pl. Plane. e. 2002. textfigs. Animal recon structions with measurements are given according to Bengtson (1970). Peterson et al.e. the canals bifurcate from three to five times..” In some Proarticulata. Brasier and Antcliffe.. dobionts. THE EARLY HISTORY OF THE METAZOA 423 d b a e c Fig.. All of this suggests that vendobionts occupy a sepa 2012). (2007). d) celo scleritesloclescleritophores: (c) Halkieria. 4–6). (d) Allonnia (Chancelloriida).e. hyphae of fungi. Brasier and Antcliffe. progressively decreasing in diameter. 2008. 2004. i. which at comparable length are sub BIOLOGY BULLETIN REVIEWS Vol. 2008). had nothing in common with the cylindrical 2004. b) – “tommotiids” (a) Paterimitra.. (b) Camenella (c. 2005. Vinther et al. Conway Morris and Peel (1995). al. the as well as the tubelike chambers characteristic of ven system of tubes is combined with canals (Ivantsov.. including the affinity and the presence of photosymbionts (Grazh “head” in Proarticulata and Bilateralomorpha dankin. Both systems are of the closed type. with which they are sometimes compared (Retallack. Cambrian (a–u) and Ordovician (e) Lophotrochozoa: (a. Like (Ivantsov.g. 5 No. Dickinsonia. fig. because the continuous fractal pattern like Escher’s “Regular Division of the fractallike system of canals of various crosssections. that not communicate with the outside environment by they in fact are not connected with Metazoan evolu any kind of pores. (2014). 7). 4. 5 2015 . © Artist Vsevolod Abramov. they are not directly related to fungi or lichens. Bengtson and Hou (2001). The of the sediment excludes their possible algal sensu lato canals uniformly fill the entire body. as they approach the wise. Peterson et al. 2003). Seilacher. i. (c) annelid Plumulites (Machaeridia). surface. 1. they do rate position among multicellular animals. 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 et al... 2003). Larsson et al.

and relief directed the water current along the body sur Schulz.. 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. Sperling et al. The carbon isotope anomalies phore of brachiopods. Nama surface area to be decreased and remove the organism calathus has a calcareous skeleton in the shape of a from the substrate.. isms. In the event of an exhausted chambers allowed vendobionts to absorb dissolved resource.. engulf interesting. Zhuravlev et al. 3a.. 5 No. precipitated organic suspension or bac organic matter forming compact multitiered bottom terial mat. megabacteria. Wood et al. this microstructure is not reduction of the surface (Brasier and Antcliffe. the significance of the first of these factors and a sharp Suspension feeding required a constant. Bab Vendobionts lying freely on the bottom and those cock and Ciampaglio. bend bionts began in the zone of counter currents and ing parallel to the current.. or fossil traces. Kikumoto et al. sky and Bengtson. All of these earli the concentration of different elements (e. absorb more water into the cells and increase their vol Sinotubulites is a cylindrical shell of irregular layers of ume. 2000. An unusual. which is determined by This system of canals. They could eccentric calcareous cones nested within one another only appear if the organism was very tightly sucking on and with closed bases. 2011). the microstructure of the skele the substrate by its entire surface. 2014). Suvorov used by predatory fungi. than a third of their length (Ivantsov and Mala sponges and Cnidaria (lower Metazoa). 2005). A change in osmotic pressure would allow the Vinn and Zaton. 2002.. relatively increase in the significance of the latter led to a com strong (over 5 cm/s) current. 2000). 2009).g. discrete ton is primitive and is found in red and other calcare movement of vendobionts to a distance not greater ous algae (Viridiplantae). 2008). would be sufficient. Chen 2001). and suspended (Burzin et al. none of these records living in the subsurface growing through the substrate meet the above morphological criteria. 2007). canals. fig. whereas this ratio in osmotic megabacteria other giant osmotrophs are characteristic of the Edi reaches 1 × 101 mm–1 or more.. Lafamme organic matter in the Ediacaran ocean was 2–3 times et al. 1993. 1998. 2013. or sometimes inorganic struc 2002. Chen et al. 2014). as well as a slight including pogonophores. H. even a small current or low waves characters are observed (Grotzinger et al. For instance. The fungal activity is initiated by a change in et al.. Ivantsov.75 mm (Lafamme et al. N and organic enable the organism’s growth. It is no coincidence that 102 mm–1.. reduced the load of the cur upwelling of the subpolar sea (Fedonkin. such a signal would be also detected by a communities (the upper tier reaches 2 m) in environ vendobiont. the most common of them.. 1988) and not in the Earth’s subsequent history.. 3b and 3d). Conway Morris. 4). 2002. The current rate dropped due to with frequent drops in the oxygen level and the the relief of the lobe. 1960. 2007.. chambers and frondlets.. has a very unusual skeleton consisting of canal system (Ivantsov..D... in annelids. 2. They either or even through adjacent (already dead?) individuals represent the remains of normal Phanerozoic organ were also osmotrophs (Grazhdankin and Seailacher. ments with very slow currents (not more than 1–5 cm/s) The content of dissolved. colloidal. 3c.. were apparently performed by the same systems of but a basal opening is present (Cortijo et al. whereas the resulting vibration of the lobe.1 s) to ella and Majaella are possible skeletal vendobionts. exactly like stalked taxa (Figs. The diversification of vendo face.e. are concentrated in upwelling zones. 2004. because they are organized tures. the largest chanical experiments with plastic models of lobelike osmotrophs. A similar mechanism is presently Namapoikia is a shapeless honeycomb mass. although their size does acaran: bacterial colonies and fungi (Marusin et al. A decrease in mass along the lobe increased (Singer et al. found. not exceed 0. 2014) (Figs.g. 1972. foraminifers (Rhizaria). The morphology of Ediacaran skeletal organisms is Traces of vendobionts are traces of absorption. quently mentioned (e. recorded for the deposits of this age suggest a large whereas the suspension feeder should be positioned turnover of the carbon cycle. threedimensional filter plete disappearance of vendobionts at the Ediacaran– ing organs (flagellate chambers of sponges.. ShieldsZhou and Zhu.. 2010. which are able (in 0.. 5 2015 . by changing the osmotic pressure in the with three lobes (Vologdin and Maslov. which the proportion of the isotopes of Ca. In the modern oceans. khovskaya. e. Droser et al. No stolon or polypoid face to volume ratio. C/N) in est skeletal organisms disappeared at the end of the BIOLOGY BULLETIN REVIEWS Vol. as is sug rence of vendobionts from younger deposits are fre gested for vendobionts. For further movement at the sur porous polyhedron on a stalk. H. ing. 2002... retain a body area to volume proportion of 1 × 1000 × 2013. Biome 2011). Ghisalbert et al. 2013). rent and at the same time boosted the exchange of flu Lafamme et al. 2012.g. higher than the present level. 2012). Kouchin hyphae quickly (Heintz and Pramer. i. 2011. stalked vendobionts in tanks showed that the “quilted” in conditions of a stable biogene flux (Schulz. which has no equivalent perpendicular to the current (Vogel. No protoconch has been found in Cloudina.N. while the mixing of the water absence of bioturbators and predators. gills and bivalve siphons). allowed vendobionts to carbon (Fike et al. 2008. catching and immobilizing a round worm or a aragonite.424 ZHURAVLEV divided by septa. Anabarites is spirally coiled conical shells water bear. 2012). This branching system of canals/ the environment. and 3e–3i). and the showing of imprints of the branching Cloudina. pl. lopho Cambrian boundary. Although the occur bent along it (like thalli of ribbonlike algae). Zhuravlev et al.

Namibia (Brain et al. White Sea Region. THE EARLY HISTORY OF THE METAZOA 425 Ediacaran–beginning of the Cambrian period and. brachi BIOLOGY BULLETIN REVIEWS Vol. mon even with the subsequent Cambrian “explosion. usually a porous cup with vertical and/or horizontal porous septa connect Sponges: Not Spicules Only ing walls in tanks (Savarese. 1994) 2009. material on heteractinids (fossil sponges) with skele The tube itself... but the assignment of these fossils to sponges. though not diverse. Cnidaria: Where the Jellyfish Swam? The sponge record begins in the Cambrian Period Most Ediacaran organisms have previously been with the appearance of Hexactinellida. 1). and Vaceletia molecular remains “of their ancestors” (Love 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. New spongelike organ netic analysis of microRNA (Sperling et al. 1993b). 1989. 2007. 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). the assignment of Namacalathus (see below). was the reason behind their assignment to a separate has a fractal structure of canals typical of Osmotro order within the Calcarea). illustrations of the spi the ends. 1996). have nothing in com cies known from the Middle and Late Cambrian beds.. 1993. biont similar to Palaeophragmodictya spinosa Botting and Butterfeld (2005) collected interesting described in the same locality by Serezhnikova (2007). Their skeleton was com (2002) recorded spicules in the cryogenic dolomite posed of dumbbelllike elements with stellate plates on Noonday (750 Ma) in Nevada. 719). which more likely sug Calcarea. although all early occurrences of ments toward improving filtration (Zhuravlev. specific tions and in relationships with related and unrelated for this group and abundant in the Ediacaran oilbear organisms). but this paper is often outer and inner walls..g. Hemispherical radiocyaths were the largest belong to algae (Stramenopiles) and are diagenetically abundant. which is possibly a stalked vendo 1986).. tible remains of some aromatic and aliphatic hydro and the nature of asexual reproduction and immune carbons (Peters and Moldowan. It in hexaactinellids and calcite tertraradiate spicules are has a prefect tetraradial arrangement of spicules of the typical of the calcareous sponges. et al. 2006)). symmetry type and chemical composition. suggest that sponges could ern sponges. 2012) was a sponge. with only two spe light their unusual morphology. and Calcarea known from spicules of a certain sea pens (Octocorallia) (Glaessner. 2010) and isms continue to be reported from ancient beds: e. Their only equivalents and cited as a primary source (Müller et al. 2013). body plan. do not exclude the possibility that these are archaeocyaths. Summons reactions (fossil reefs retain skeletons in lifelike posi et al. It is difficult to imagine that the Ediaca Since the hexaradiate siliceous spicules are found only ran Coronacollina (Clites et al.. which is a Palaeophragmodictya speci tons composed of regular multiradiate spicules (which men from Ediacara Hills (Gehling and Rigby. in which the stellate plates were over graph of a “speculate sponge” from the Vendian of the time replaced by solid rhomboid plates (Zhuravlev. Cambrian Period: heteractinids and archeocyaths. Demospon considered members of Cnidaria. 2008). Only Homoscleromorpha whereas Ediacaran “jellyfish” represent vendobiont are not confirmed in the fossil record. 2010). Cambrian reef builders altered (Antcliffe. 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.. as well as 1992). p. 1992). 2007. mainly jellyfish and giae.e. 1984. which. This hypothesis was supported by phyloge gests a mineralogical origin. 2007. (Zhuravlev. The same authors published a photo receptaculids. which include taxa with calcareous skel have existed 635 Ma (Love et al. 5 2015 .. Acanthochaetetes. 2011). In contrast. some The latter were the most prolific and became largely of them were fossil traces (Jensen et al. 2002). 2009). It is quite possible that these biomarkers (Fig. in extinct within the Early Cambrian. 5 No. archaeocyaths to sponges is supported by biomechan ical studies of skeleton models. formed porous cules have not been published. Biomarkers (indestruc Judging from the skeletal microstructure. these organisms are debatable. complete skeletons (Fig.. 1). 24isopropylcholestanes. 2013). Reitner and Wörheide of supposedly sponge affinity. remains unsubstantiated. Debrenne and Zhuravlev.. i. Cambrian “jellyfish” were more diverse. also by the appearance of spicules in calcareous unusual.. similar to the skeleton of Love et al. etons with no spicules.. 2012). 2010b) and Otavia in rocks from 760–635 Ma in Wood. The authors found in the pha–vendobionts rather than sponges that are suspen earliest heteractinid Eiffelia bilayered hexaradiate and sion feeders. 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. attachment discs or colonies of algae and/or bacteria there were several extinct groups of sponges in the (Grazhdankin and Gerdes. Serezhnikova.” Since both were suspension feeders. or to the Metazoa in general. Jenkins. in which the Olom Formation of Mongolia (Brasier et al.. by contact with rays. 1). Sperling probable descendants were Ordovician–Permian et al.. Late Ediacaran spicules from the Tsagan tetraradiate spicules of several orders. However these “sea pens” are vendobionts. archaeocyaths were most similar to mod ing and carbonate deposits. However.

modules. Demospongiae. Vinn. Moreover. a multilobed. 2006. Cart sent the remains of of nonclonal organisms capable of wright et al. Zhu et al. Sennikov.. all of the earliest representa ilies (Hydrozoa. For instance. For instance. 1998). 2014). are found in Lagerstätten and phosphatized) skeletons in the shape of an upturned lithified reefs (Rigby and Hou. Their affinity to any extant groups is organisms in each major branch of Bilateria—Ecdys not established. 2013). paropsonemids. if tetraradiate symmetry is bryozoans—2. 1997. although statements to the contrary ozoa. 2007. i. coralomorphs—25. Possible jellyfish imprints are no connection to the origin of Bilateria and Metazoa.. Lophotrochozoa and Deuterostomia—repre can be found in the literature. and conu 2008.. Kruse and Zhuravlev. 5 No. swimming disc. pter Sphenothallus. However. For instance. 1985). a fossil group that had and Briggs. Zhu et al. In other words. the possible Cnidaria included Hexaconularia appear... Conulariids appeared in 3. 2007. at deposits that in the live animal gradually lost their con least 30 Ma earlier than the aforementioned Middle nection to one another. 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. described movement. they were modu ual.. they consist of three modern classes or not a jellyfish at all. or with Coronata. Dewel consid extinct Ecdysozoa (Anomalocarididae) (Whittington ered sea pens to be Vendobiota. sea pens.. Xenusia (Ramsköld and attachment discs and pseudocolonies in the two latter Chen. Dong et al. some Olivoodes and “soft corals” have a pentaradial symmetry instead of tetraradial. 2014).. the first fossil Hagadorn. 1992.e. 2004. al. 1993.. another 400 genera were described. a represen ever. only skeleton covered on the top. 2014. even among confirmed fossil jellyfish representing three modern classes and four fam sponges and cnidarians. radiocyaths. which does not exclude (With and without Inverted Commas) their possible affinity to Ecdysozoa (Liu et al.. Their complete skeletons. known only from the Middle Cambrian (Young and If the fossil record is taken into account.. which are only known from the lins. 1999. like the history of suspended spirally coiled gut with a crown of branch Sponges. as Deuterostomes well as micrornamentation. or probably chitinized. and Cubozoa).5% are modular taxa (archaeocyaths. Rigby and Col hexagonal pyramid). after 10–15 Ma. pared to Stauromedusae.. The same group of jellyfish pre were hemichordates. but not all modular organisms can be con sidered colonial. even if they developed by Cambrian “jellyfish”. represented by phosphate tubes with obranchiates appeared only inthe Middle Cambrian. whereas the earliest archaeocyaths were solitary organisms. Hexaconularia include no more than 5 are modular. Harvey et al. 2000. Although a third of Cambrian modular organisms Steiner et al. massive (multimodular) taxa (Wood et or the position on the bedding surface. The same applies to the Cambrian speculate lar forms similar to Ordovician corals (Tabulata) sponges (Hexactinellida. Apart from record. if (Wood et al. 2002).. pelagic organisms with taxa suggests their cnidarian affinity. possibly chitinized. and hexaconoluriids are com and other sponges—75 genera. with mineral and chinitized the modules are separated by secondary skeletal skeletons. based on 120 specimens. In general. None of these taxa is an early ancestor of Olivoodes and resemble juvenile coral polyps included any group of Metazoa. graptolites and pterobranchs—48) considered as a major character. 1995. 2011) (Fig. 2006). 2001).. 1). 1989.. in the peridermis (Bengtson and Yue.. 1993. The term “modular” is used here because this is either a species combining characteristics of all all colonial organisms are modular. but their microstructure and the presence of colonial organisms (Maletz. and only much later do very rare modular taxa these. In the last strobililike constrictions are taken into account decade. the earliest Deuterostomia were sumably includes the hyolithelminthes Byronia and not colonial organisms. 2005. Park et al. of the 4367 genera lariids with a fourfold organic. 1992). contradicts Dewel’s (2000) hypothesis that ing tentacles around the mouth. basal Cambrian of South China and India. 2009). of which (van Iten et al. 1992. Among hemichordates.. 2014). so their total proportion some Cambrian embryos known as Punctatus and decreased. Zhuravlev. “Rhabdopleura” and Cephalodiscus(?) (Durman and van Iten et al. appear only in the Cambrian Period. Zhuravlev. and The history of Cnidaria. the colonial organization of which gave rise 2002. 2010). later. i. 2012). in most archaeocyaths. How tives are solitary organisms. animals compared Bilateria could have evolved from clonal animals like with lophophorates and deuterostomes (Friend et al. The earliest Cnidaria. They were at first very simple branching or budding from the same paternal individ singular organisms. the Late Cambrian. 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). and even the mouthparts of to the triblastic ancestors of Bilateria. 5 2015 .e. Calcarea). of Cambrian fossil organisms known by 2001. Scyphozoa (2). transverse ribbing and microlamellar microstructure and the earliest of these are very simple solitary taxa— common in the Cambrian rocks (Bischoff. Ivantsov et al. Fuller and The solitary forms are the first to appear in the fossil Jenkins... 2010). not disassociated (sessile organisms with phosphatic (or postmortem into separate spicules. A further increase BIOLOGY BULLETIN REVIEWS Vol. Wu et al.426 ZHURAVLEV opods (Zhang et al. Their aggrega These are often compared with annelids or pogono tion presumably resulted in the appearance of simple phores. (Zhuravlev et al.

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

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

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

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

Malakhov and Andrianov. xenusians include species with a retract ment of muscle facies associated with the cuticular able proboscis. begins as paired dorsal ganglia. Huang et al. The transformation of a highly specialized cida (earliest cephalorhynchs). able proboscis was similar. Legg et al. is impossible biomechanically: the locomotion logically organized and structured to those in xenu of such worms by hydraulic pumping and coelomic sians (and onychophorans.. and with segments and a mouth cone like that in Cambrian appendages clearly unsuitable for locomotion but suit cephalorhynchs (Omnidens). 2011b) (Fig. Hou et al. 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... embryologically terminal and that the antennae the presence or absence of the neck. burrowing organisms adhered to by almost all authors (Dzik and Krumbie (Facivermis) with anterior lobodialike appendages gel. 2013b).. although in the latter the fluid distribution is only suitable to move within the cuticle is not phosphatized). and third segments. 1989. 2014): these are the crustacean labrum. loriciferans.. 2009. antennae and eyes in some xenusians. 2007. 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. and nematophorans. tral taxon of this group can be interpreted as a vermi 2010). 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. et al.. originally described upside down and back to front... The latter are ated lobopodia and proboscis and with a terminal known from beds over 525 Ma as larval skins (Xenu mouth.. retain characters of palaeoscole fact the paired spines are on the back. and a vermiform posterior region (Liu et al. although not found as fossils. In Daley et al.. Some Palaeoscolecida substrate. Dzik and Krumbiegel. 2003). Such organisms present as one of the common sion. Thus. 2012b). or simply animals with spines.. Peel. 2011b. Reverse evolution— able for anchoring in holes (Mureropodia) (Gamez from cephalorhynchs to xenusians and arthropods—is Vintaned et al. This (Zhuravlev et al. 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). Zhang and Briggs. which was vae of priapulids. whereas the first confirmed cephalorhynchs lobopodia (Dzik and Krumbiegel. THE EARLY HISTORY OF THE METAZOA 431 mary innervation of the antenna remain unresolved. pedum common in the basal Cambrian. (Palaeoscolecida) appeared no earlier than 525 Ma Gamez Vintaned et al.. as in cephalorhynchs. 2011b.. Liu et al. There are confirmed whereas the antennae are innervated by deuterocere records of burrows of Cambrian cephalorhynchs con brum (Ou et al. which starts as a paired organ simple Ushaped burrows (Fig. 1989.. 1995. 2a) or deadend. 2005. 2011) (Fig. 2011b... Others think that the son. jaw. 2012b). 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. Ou et al. 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. 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.. Caron et al. 5 2015 . mouth is formed anew by shifting derivative labial 2006. Kinorhynchs. Based on the presence of completely different cuticle and mouth apparatus. Kimm and Prpic. 5 No. 2010). 2b). 2006. which are assigned to than 535 Ma as phosphatized claws and cuticular Xenusia... 2010. cephalorhynchs as “priapulids.. 1996. 1986. 1993. which have Based on the onychophoran ontogeny. 2011.. 1989) and from beds older Cambrian ecdysozoan groups. Budd. 2003) but et al. BIOLOGY BULLETIN REVIEWS Vol. Maas et al..” although they have a Martin and Mayer. 2a). 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. 1998. it is possible to these taxa include gigantic animals with a mouth more suggest that the brain of xenusians with a nonretract than 0. The evolution from worms with a retractable retained reduced paired lobopodia on the ventral sur proboscis to onychophoranlike organisms is not in face. 2014). (Maas et al. 2006. 2011. The lar group includes the famous Hallucigenia. Harvey et al. 1). Zhuravlev circumpharyngeal origin (Eriksson et al. by the protocerebrum and are hence homologous to Zhuravlev et al. Many authors still refer to all fossil tritocerebrum is not formed (Strausfeld et al. 2009. 2006). 2014)... 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. have a serial arrange However. there is no evidence suggesting that form organism with paired retractable undifferenti cephalorhynchs preceded xenusians. apulids and completely unlike false traces Treptichnus 2006). the ances been interpreted as priapulid burrows (Vannier et al. whereas the cids and their larvae in the structure of the cuticle flexible appendages are paired walking limbs. Tardipolypoda. Liu et al. in and even their adults. Zhuravlev papillae of the antennae. whereas the Cambrian) (Fig. 2007. Zhang and Pratt. Budd and 2001.2 m in diameter (Omnidens)..

a pre 2007).. among organs (Dewel and EibyeJacobsen. For example. from the lobopodlike appendages in the higher degree Zhang and Briggs. 2011. paired preoral appendages. Storch et al. which were most likely to be innervated near the anterior gut is found also in priapulids (Meio from the protocerebrum. 5 2015 . 2006). Halberg xenusians. and chordates with a head shield. they are adapted to Telford. 2003. Yang et al. later ganglionized ventral chain (Whittington and Kinorhynchs are worth mentioning again Mayer. almost et al.. Daley and Edgecombe. Tardigrades stylets are derivatives of the various species of anomalocaridids and xenusians lobopodlike limbs that were transformed into inner crushes all cladistic schemes. approximately as in Diania Xenusia et al. and some other Cambrian cephalo apparatus and in some taxa (Kerygmachela and Tami rhynchs suggest the presence of a controlling structure siocaris). Hou et al. 2009. also accommodates Opabinia and Nectocaris. proboscis. 1985. 1998. Whether or not Articulata is a “natural ” group. Bergström et al. arthropods. 2001). which connects the contrary. Anomalocaridids with preoral SchmidtRaesa. which were extinct in the Devonian Period.. a head shield the ventral somite into sternites and tergites. in cephalorhynchs (radiodonts or dinocarids).. the mosaic combination of characters in and cuticle.. or acquired Peytoia. 1989). because fossil inhabitants of the Cambrian seas. Hou et al. 2011) 2001) (Fig. anomalocaridids. This group (Fig. 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. 2d). and external gill including cephalorhynchs (Eriksson et al. sometimes of several orders. Ma et al. The origin of Another group likely to be associated in its origin Pycnogonida is not certain (whether they are true with xenusians—anomalocaridids (Anomalocaris. Second. 2003. On the verse muscles to the serial fascia. up to one meter long Cambrian and Jurassic taxa have features of organiza (Figs. 2002. a body with entiated cylindrical walking limbs with numerous swimming lobes possibly bearing respiratory fila smooth podomeres.. 5 No. differing (Whittington and Briggs. 1970. They have a proboscis with radially tion of the head section like those in xenusians arranged tooth plates. 2013. 2009. Melnikov et al. Paterson of sclerotization. closely related to chelicerates. and partly tardigrades. 2014). the preoral lobopod appendages (Bergström that is similar to the mesentherium and hence the and Hou. 2006. 2e). 2009).. 2011): xenusians. 2h). 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. based on the mouth palaeoscolecids. 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.. 2007.. as (Waloszek and Dunlop. This but instead developed independently in several groups process is connected with the functional differentia of Ecdysozoa (Ponomarenko. is observed in the Cambrian appendages with claws and a head region with traces of xenusians Hadranax and Pambdelurion (Budd. and a caudal region with or without cerca and (Chen et al. undiffer sometimes composed of several elements. 2006. 2009). large compound region but with true antennae. BIOLOGY BULLETIN REVIEWS Vol. Amplectobelua. in addition to four (Zhuravlev et al. coelomic cavity (Zhuravlev et al.. 1992.. because a reduced coelom appendages. as is considered in the kov. resulting in the bilateral appearance of segmented appendages and a head region without triradiate mouth apparatus. 2013). 1995b. a second specialized eyes (up to five in number). Charbonnier et al. 2011).. the dants of xenusians that adapted to nektobenthic active distinct axial position of the gut in xenusians. they lack the definitive charac meiobenthic habitats and thus have acquired a simpli ters of arthropods. predation and active filtration. 2011b) (Fig. whereas the earliest Middle Cambrian (Fig.. whereas Mureropodia has an introvert and tardigrade has paired rudiments of the lobopodian reduced lobopodlike appendages with claws appendages in the head region. Apart from that. tagmosis and a reduced proboscis (Ou et al.. 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. First. can be considered descen priapulus. Antennacanthopodia had lobopodlike limb to the cover plates. vetulico of the ventral nervous cords into the segmented and lians. as than the homologous prostomium of annelids (Melni the basal group for arthropods. filaments (Fig. and others)—are the largest a segmented skeleton independently). 2b). the It does not seem correct to consider anomalocari labrum of arthropods develops as a paired organ rather dids. 2008. 2011. 2006). Daley et al. Daley and Peel.. oral of xenusians as the ancestral group of Ecdysozoa.. 2f). Mounce and tion of limbs and apparently with the transformation Wills. similar to the optical pair of segmented appendages and differentiation of organs of the most derived arthropods. 2g and 2i). Arthrodization and pairs of locomotory limbs and Cuticular plates like arthropodization did not necessarily occur together those in xenusians (Maas and Waloszek.. Tardigrades are sians and true arthropods (Euarthropoda) (Budd and also their possible descendants. Ma et al. 2011b). 1).. Kimm and Prpic.432 ZHURAVLEV Xenusians represent a stem group not only for cladograms in which they are placed between xenu cephalorhynchs and onychophorans.. Diania have strongly cuticularized. 2006. Tanaka et al. a straight gut with serial paired digestive diverticulae 2012. (SchmidtRhaesa and Rothe. and a rounded distal segment ments. 2014) (Fig. as in some xenusians. 2010).

Why would least one of four specimens in both genera. 2008. including the limbs (Balavoine and Adoutte. 2012). ochaeta. (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). and dorsal or ven eta (Vinther et al. (Fig. i.. 2007). 2011) phora (Urbanek and Mierzejewska. Ivantsov. groups appears to be determined by the fact that On the whole the fossil record of early annelids is arthropods. 2008.. some Cambrosipunculus from Chengjiang (Huang et al. if the inter mediate forms between different groups of Ecdysozoa Other worms belonging to Lophotrochozoa are not found in the Cambrian.. It is not surprising that they were recently Ordovician beds. Vinther and Briggs. 1979. 2007. imprints of their cov cles of the introvert structures found in Palaeolescidae ers. while the “retract stem group for arthropods (Mayer and Harzsch. annelid taxon. the Triassic (Vinn. Vinn et al. Moreover. Struck et al. 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. the fossils them diate forms. Canadia. there were segmented taxa with calcareous characters can be assigned to any extant group: they elytra (Machaeridia) covering the parapodia with cha lack antennae. 2011b). idae) are most interesting from the point of view of the BIOLOGY BULLETIN REVIEWS Vol. with thick.. retained a certain set of origin of chaetae as external defense elements in characters of the common ancestor of Bilateria. wormlike locomotion developed. The first polychaetes. the micro dia (noto and neuropodia) (Conway Morris. lians. and annelids. However. 2011). had exactly this “horrent” look.g. the covers devel Nielsen (2003). whereas reliable Sedentaria assigned to mollusks and to aplacophorans. 4e).. The com arthropods and priapulids–nematodes). 2008. 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. motile epibenthic taxa. Butterfeld. only one. 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. 2011. In fact these are ribbed remains of motile polychaetes with bifurcate parapo organic tubes of problematic sabelliditids. 2009). Whittington and Mayer. 2003. and are also abundantly found in the Lophotrochoans: same bed in Chengjiang.. and the palps are very simple (EibyeJacob The elytra of Machaeridia are similar to the shells of sen. 2006). more precisely. Although Archaeogolfigia and in the fossil record are found in abundance. was of some polychaetes were considered as such interme proposed by Struck et al. 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. or. Vinther et al. not the earliest. 2009). 2004.. in all Ecdysozoa(!). 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. forms. None of boniferous annelids crawling on the surface of the sub the Cambrian annelids with their combination of strate. 5 2015 . They are exclusively represented by the occurrence of Pogonophora. 2006. among the Ordovician–Car particularly motile (Merz and Woodin. 1983. Per 1990). Errantia and Sedentaria. as Prpic. tral setae. THE EARLY HISTORY OF THE METAZOA 433 2006).e. able pharynx” was the attachment disc (Dong et al. 2). The straight. representing Ecdysozoa.. like the intermediate change between distinct branches. Vinn and Diverse polyvalved taxa (Halwaxiida or Halkieri Mutvei. 1). 2012). structure of which is distinct from that of Pogono Conway Morris and Peel. “posterior” sec the only Skeletons in the Closet tion of the gut is in fact imprints of the retractory mus Annelids. The literature on the Edi they are a thousand times less common than cephalo acaran and Cambrian period still has references to the rhynchs. Later. are completely the terminal group of sipunculids. which Eibye absent in the beds (for example. the body surface of these worms clearly shows scalides and sclerites like those in palaeoscolescids. although (Zhuravlev et al. 2008. 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. However.. e. 5 No. whereas the paired ventral nervous chains in Imprints of earlier annelids.. fig. which could have been considered intermedi 2004) have already been suggested as representatives of ate between annelids and arthropods. 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. EibyeJacobsen and Vinther. supporting chaetae. 2009). Scole Polyplacophora and diverse Cambrian “polyvalves” codonts (fossil jaws of polychaetes) appear only in the (Fig. a good illustration of Westheide’s (1997) theory of the representing Lophotrochozoa. 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. hooklike setae was probably not It is interesting that. The similarity of both 2008. are also found in the Cambrian beds. Williams et al.

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

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

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

Szaniawski. and the calyx is covered by rounded sclerites. 2004) and their unique genome morphies is the spiral determinate cleavage with sepa (Marlétaz et al. sipunculids. All of these groups apparently repre 1983. and could and ctenophores. with two logarithmically coiled supports (helens) polyplacophorans. and to form a brain (annelids. 2010. Penner 2000. 2007) 2014).. echiurids. is com but have serial paired muscle scars as in monopla monly found beginning from the basal Cambrian. and stenothecoids. This fossil is externally similar to Kamptozoa (Zhang which later evenly divides to form the incipient bilat et al. 1975.. which survived until ans.. 5 No. 2008). than any extant kamptozoan (5. 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 (β or γchitin) chetae secreted in saclike invagina Hyolitha and Stenothecata (Runnegar et al.5 cm instead of 1 cm). 1). 1976. 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. sipunculids. brachiopods. 1996. ing in the conical valve but also for controlling the muscles of the appendages. 1). The sclerites resemble mobergellans. and juvenile cephalopods. They probably just lay on the The Cambrian also yields remains of chaetognaths substrate.. 2004. 1995). Feng et al. The combination of the operculum and appendages exclude the presence of a And Many Others muscle foot in hyoliths. only for the tight closure of the shell by slightly retract Giribet et al. it is significantly larger erally symmetrical mesoderm (annelids. 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. nemerteans. phoronids. less well known. echiu Cambrian Lophotrochozoa include another three rids. 1996. and Early Cambrian siphonoconchs. which is suggested by occurrences of oriented shells of Chen and Zhou. rate micromere 4d. 1997) (Fig. The shell in true hyoliths blasts) with microvilli capillaryshaped. 2002). traces of was composed of a large conical valve and an opercu which remain (annelids. Meyer et al. camptozoans. were more closely related to mollusks (Kouchinsky.. and mollusks. The third. 5 2015 . myzostomids. Gline et al. One of the most important synapo logenies (Halanych. (Parkhaev. However. 2013) (Fig. 1999. phosphate rounded layered shells slightly resembling which is retracted during metamorphosis into the inte larval brachiopod shells. it served not are homologous to chetae) (EibyeJacobsen. Maslakova et al. 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. based on the shell microstructure. whereas both region of the gut are straight Chaetognaths are very rarely found as complete in hyoliths and juvenile orthothecids (Devaere et al. 2001. 2011. bryozo representatives groups: hyoliths. supported by the appendages. appearing at the stage of 64 cells.. 2010. Rozov. lack appendages and are commonly found buried vertically. paired protonephidia.. in nemerteans and the Permian in a much more impoverished state than brachiopods there are only cell homologues of the pro in the Cambrian. Rouse. number of combs (Conway Morris and Collins. myzostomids. the trochophore is considered to have been coids. BIOLOGY BULLETIN REVIEWS Vol. superficially resemble brachiopods more than bivalves known as protoconodonts (Protohertzina).. 2008). ciliated tuft. Other hyoliths. in which chitinous teeth in the stomach tem of muscle scars on the operculum. and apical plate. Hyoliths lost in cephalopods mollusks and clitellates) (Funch. group of Cam These remains differ from true conodonts and other brian lophotrochozoan “bivalves” is the class chordates in the microstructure. organisms. as well sealed with the operculum. Vannier et al. imprints (Chen and Huang. The early appearance of cha sent an early radiation of Lophotrochozoa. 2012). 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). cophorans. 1984). rior.. The phoronids. Zhuravlev and Wood. storfer and Scholz. THE EARLY HISTORY OF THE METAZOA 437 and an aboral anus ringed by 30 marginal tentacles. cycliophoran... The most interesting hyoliths in living position on bedding planes (Kruse is the discovery of Maotianoascus represented by both et al. this is lost in brachiopods authors who described this species assume that kamp and bryozoans. and mollusks. Martí Mus and Bergstrom. Early–Middle Cambrian stenothe totroch. 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. lum. Lambert. 2002. 1998). In light of the complex sys as bryozoans. Stenothecida were bivalvian organisms that (Fig.. tions of the cuticle by large epithelial cells (chaeto Sysoev. but their phosphatized dental apparatus. 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. 1). which are character Siphonoconcha. as in (Chen et al. sipunculids. 2007). although some have a different using the mantle trail or a lophophorelike structure. Synapomorphies of 2007. 2009). 2004. camptozoans. Orthothecida. myzostomids.

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. Rehbachiella). from the Burgess Shales and other Lagerstätten that from several slow predators to a vast diversity of active cannot be currently placed (Amiskwia. renewed four times in the geologically short interval of including sponges. Nielsen (2012. even within the Ecdysozoa.. 2012). 1995b. They can Ecdysozoa was formed in animals inhabiting the lit have giant grasping appendages instead of antennae or toral. 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. For instance. 2013). echino the Ordovician: Late Ediacaran..3. and the mineral skeleton in different groups. arthropods. Early Cambrian. let alone tommotiids or chancel Middle Late Cambrian. with little connection to actual Fuxianhuia. (Stein et al. Tanaka et al. say BIOLOGY BULLETIN REVIEWS Vol. cnidarians. all of the first Ecdysozoa ulation can be completely absent. at 2012. 2013. from almost virgin.” The world of Metazoan organisms Previous discussion shows that Cambrian fossils. copy shows the distribution of iron and other chemical Thick.. and ostra are faulty in that the evolutionary events are not linked codes (bradoriids. p. acoelans. cian Revolution.4). Legg et al.” including calcareous spirally coiled shells of the bottom water layers to well aerated waters filtered cribricyaths. which has been treated in all phylogenetic time and space. the Devonian Period with the appearance of forests thereby showing a very fine detail of the nervous sys and mycorrhiza. 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. imprints of mate. 2009. 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. Davies and Gibling. and other inhabit diversity” but as a world of organisms adapted to par ants of ancient seas. Maloof et al. from various parts of the brain to the limbs (Ma et al. Alalcomenaeus is more similar to that in Chelicerata. new microscopy methods showed that. ducing gymnosperms (in amber). et al. 10. from a cold to warm cli ing agglutinated and secreted layers. benthic and nektonic chasers. 2013). Branchiopoda and Phyl Many hypotheses about the origin of life on Earth lopoda (Isoxys. textfigs.. among Cambrian arthropods. mollusks. 2009. crinoids. Legg et al. pro trees as a basal Chelicerata (Chen et al. sandy series began accumulating by the end of elements in clay minerals replacing the soft tissues. Canadaspis. 2009.. However. 5 No. but only in those tha became par ticular environment that essentially changed during asites.. 2001. posed a hypothesis of primary ciliated holopelagic 1995. and commonly even in their than the Paleozoic biota differed from the MesoCen nearest (Ordovician) descendants. Kouchinsky et al. 2010). cephalorhynchs or 80 Myr from the midEdiacaran to the beginning of annelids. which existed for approximately 250 Ma each. It was demonstrated that To some extent. The nervous system of stätten will produce cycliophores. Dinomischus.” not even as variations of “archaic the skeletons of trilobites. Epipodites specialized for breathing or osmoreg empty. All of these fossils ozoic. or other groups lacking any hard structures. formed independently. and Oesia) (but these are unlikely to brian “explosion” was followed by the “Great Ordovi include acoelans or acanthocephalans).. different time and in each group. whereas all head and other animals lived in a normal marine sublittoral appendages can be totally uniform.e. 2008.. orthonectids. 2013). by studying the most common Chengjiang fossils 2010a. Maas 10. favorable substrates to medusoid parapsonemids with a Ushaped gut and almost motionless and weakly attached filter feeders to tentacles encircling the mouth. 2014). represent ancestral groups or their extinct branches.438 ZHURAVLEV It is unlikely that even the best Cambrian Lager organized as in Mandibulata. the Cam Odontogriphus. a very strong destructive factor for tem up to the optical nerve and nervous fibers leading rocks (Bonneville et al. derms. and Paleozoic (formed in the loriids. 2012. Wills. 171). 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. Scientists some Despite all their peculiar characteristics. 2008. For instance. phosphatocopids). had a nervous system organisms rooted in Haeckel’s “Gastrae” theory. from the walking limbs.... Haug et al.. i. 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... whereas coastal areas a hypostome connected to the anterior pair of append were covered by sand because of the washout from the ages. 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. 2010. 5 2015 . there are several “unidentified the Cambrian: from seas with low oxygen content in objects. or chordates. etc. brachiopods. lack key characteristics occurring in the extant Ordovician) biotas differed from one another more members of these clades. 2012. In fact. and some remains strongly bioturbated sediment (substrate revolution). Vannier et al. conical shells of Solterella with alternat by the pellet conveyor belt. indistinguishable environment (Burzin et al. 2012.. forestless land. partly submerged in water.

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

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

2005. Javaux and Marshal... represent molecules. based on the molecular data and without septa. Sebé laminines. which is quite a long time. 2006. by the end ble for the development of the anteroposterior axis of the Ediacaran (not later than 0.. Por 2012). 2013) loops. Schaap. and in fungi todes. and it is also used in the mitosis taned and Zhuravlev. Amoebozoa). attractors. Butterfeld. Bonner. 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. causing aggregation and differentiation of and animals belonging to Opisthokonta: a rigid con the cell. Ger The gene complex of Metazoa apparently began man and Podkovyrov. Chytridiomycota. 5 No. perhaps cross soil barriers impermeable for solitary cells the genetic apparatus could have evolved separately (KuzdalFick et al. tive intercellular systems (ancestral Notchtranscip The eukaryote fossil record. i. including transductors. 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. 2009. 2009. E. the complex of the key Metazoan partici tional. which determines the ing pseudoplasmodia Dictyostelia. and ing a transitional stage between the multicellular fungi activators. and both are assigned to Unikonta are known from approximately 1. 2007). 2008. which are responsi substrate (Fig. although it is difficult to assign them mycetes in the section Myxomycota). 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. 1985). This is an adequate reason from them? for the evolution toward multicellurity. 2009. Gámez Vin zation of cell division. osmotrophy above the substrate surface and inside the 2007). which is facilitated by alternative traces are also identical (Meyer et al. the basal group thalli) (Fedonkin and Yochelson. group of Amoebozoa. homeobox genes (Wariai).. 2010. and Gaojiashania (Fig. 5 2015 . the Meta (Han and Firtel. 2011. Vendobionta).. Nagovitsyn. multicellular organization occurs among the pating in the embryogenesis.55 Ga). the controlling factors regulating tran Filasterea.7 Ga and (Chytridiomycota). 2002)]. which is increased during the formation of fruiting However simple the Ediacaran and Early Cambrian bodies. vary in width within the same trace. which predeter BIOLOGY BULLETIN REVIEWS Vol.e. ca. and lower Opisthokonta: amoeba Capsaspora. or by the presence on the same substrate structure of organelles.70–0. 2013). 2013).. Myxomi of fungi. communica Pedrós et al. the duration of that calcu and polarization of epithelial cells. 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. Apparently. and genes producing neuromediators iplantae. 2002. contains traces in the beds (neuropeptides) present in Choanofagellata.8–0. iidae. Another branch of Opisthokonta. record (Burzin. cell differentiation (genes synthesizing into consideration various “plant” remains (Virid tyrosinases). Filasterea (Cap nally identified as hydroid colonies connected by saspora. Suga and RuizTrillo. 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. SebePedros et al.55 Ga similar to Horodyskia (they were origi osporea (Creolimax. or aggregates of amoeboid cells. 515 Ma)).. Sphaeroforma). Torruella et al.. and Apusozoa (Amastigomas). Zhuravlev et al. sister group of Fungi (Brown et al. which are basal for the Metazoa Amoebozoa (Lobozoa) exists at least 0. Fairclough et al.. ter. 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. 2013).G. which does not take tion complex). 2008. these were relatively well thelium in Dictyostelia (Dickinson et al. Ichthy 1. 2012). 2005. 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. Sternfeld and singlecelled organisms capable of forming colonies of O’Mara.. 1). important that slime molds have migrating pseudo the assemblage of which needed a long time. 2010. Suga et al. 2006..0 Ga in the fossil (Baldauf. RUNX). H.. group between these organisms and Amoebozoa. 2011).. resulting in the formation of a polarized epi Metazoa might have looked. and can not find clear precursors of these organisms. Fedonkin. teria have a regular pattern. is considered the sister group of organisms characteristic for the lifecycle of fungi.58 Ga. 2013. of Opisthokonta. sister group. 2006). 1998). 1).. 1997. Thus. Fungi that can be recognized from hyphae with or The latter group. Eme et al. 2007. which could include up to five different types struction with a fractal system of canals suitable for (Saran et al. the synthesis of lated explosion is 40 Ma. aggrega Indeed. adhesion... 1.. form 2013. all of these organisms belong to (Wallraff. 2006). bifurcate. sexual reproduction. the best studied to extant groups. Eichinger et al. Stramenopiles). 1993. THE EARLY HISTORY OF THE METAZOA 441 as skeletons. It is developed animals with a complete genetic apparatus. cadherines and integrines). assigned to apoptosis. They and choanoflagellates. 2010) (Fig. of Choanofagellata + Meta scription (Brachyury. spores covered by a hard cover and attached by a stalk Except for Apusozoa. and cellular slime mold Fonticula from Nuclear ization of cells in tissues (genes synthesizing catenines. and polar zoa. The mineralogical and and production of protein necessary for building a elementary composition of the globular structure and tubulin cytoskeleton. and Wallraff. shows diverse signal Metazoan The first vendobionts appeared 0. (Fig. 1.. If we can plasmodia. Ministeria).

gametes. 2004. 2004) (Fig. Carr members of Ecdysozoa (xenusians... 2010. heteractinids. et al. Lophotro chozoa (tommotiids. the PreCambrian. However.. and all Cambrian fossil embryos belonged to direct developers. Cartwright. annelids. which are proposed as liffe. is development in the Metazoa. In the unicellular Opisthokonta and a pipette is commonly searched for in those hypothet Dictyostelia.. Collins. 1998. as well as an explosive growth zontal tunnels.g. hexaconylariids. Vendobionta). BIOLOGY BULLETIN REVIEWS Vol. and sponge cho dants of organisms resembling migrating slime molds. Suga et al. Opisthokonta are characterized mostly by clonal and syncytial colonies. in some specialized planktonic filter welldeveloped attachment disc (Brasier and Antc feeders. and later—bryozoans). including hori natha (protoconodonts).... Such a confluence of two life stages would Peterson et al. on the surface of the substrate inhab kamptozoans. because molecular clock data. Choanoflagellata. 2008. 2003. cellular Opisthokonta. simultaneously provide an opportunity for metazoan Chernikova et al. we see genesis and therefore are not homologous to choano here the almost synchronous appearance of primitive cytes in Choanoflagellata (Maldonado. 2013). by the integration same type of frondlets. such regulatory mechanisms begin oper ical ancestors of the Metazoa that could not be fossil ating during colony formation. pycnogonids.e. hemichordates. stenothecoids. Chen et al. drastically different molecular histories of of movement). SebéPedrés early cephalorhynchs and arthropods. Cnidaria the presence of the Metazoa and even the Bilateria in (corallomorphes. This sequence of events does not agree well with The surface tracks are particularly interesting. 2003). but the genetic toolkit responsible A Gastraealike metazoan progenitor would be for cell adhesion and polarization and a cascade of improbable. and possibly put forward. ancestry needs to be refuted and a different scenario ancient mollusks. 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.g. RotaStabelli et al. (Gámez Vintaned andLiñán. The extant basal ized. 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. 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. halkieriids and other celoscleri Thus.442 ZHURAVLEV mined the Cambrian diversification. Haeckel’s Gastraea.55 Ga. as well “make” a multicellular organism out of a conventional as system biases (Ayala et al. e. Traces of organisms similar to (early groups of echinoderms. 2013). 2011. To many other assumptions of molecular biology. hyolithelminthes. at the very end of the Ediacaran and later—conulariids and medusoids). which gave birth to all the sedentary stalked frondose Charnia masoni growing other Metazoa. Calcarea and Silicea 1.. large planktonic and deployed in aggregative amoeboid colonies (Sebé nektonic organisms did not exist at the beginning of Pedrés et al. slime mode organism (an amoeboid aggregate capable Therefore. the only distinct evidence of (archaeocyaths. Bromham. and probably left by an organism with appendages. later tardi et al. into a big one (up to 1 m high) Charnia grandis with a However. 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. indicating that they were statistical methods for primary data processing. Assuming that Metazoa are possible descen divisions that are not synchronized. 2004. and slime molds are found on substrate surfaces dated chordates).” i. These could indeed a hypothetical metazoan progenitor. 5 2015 . and Chaetog (<0. grades. the epithelium formation. 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. 2013).70–0. brachiopods. Deuterostomia ited by slime molds. (2009. and vertical traces of their diversity (Fig. i. and others). Ctenophora. 5 No. 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.. anocytes arise from noncollared cells during embryo the Fungi could be descendants of its fruiting stage. a number of represent an extinct intermediate group of the multi important gene complexes have been apparently lost.. e. the hypothesis of a planktonic filter–feeding tophores. Fairclough et al... since the planktotrophic larva was a late gene modifications.55 Ga). 1.. the Cambrian. 2013. hyoliths. which was developed recently by dobiont fossils from the Trepassy Formation of south Mikhailov et al. 2010. surface tracks/trails.e. the selected left by a body in between). anomalocaridids. and pentastomids). 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. Ven of a synzoospore. 1). 2007. 2007. Moreover.. 2013). siphonocochs. being neither fungus nor meta whereas colony formation is carried out through cell zoan. Therefore. 764). p. followed by multicellularity. Yang. are marine trace fossils.

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