The Wengrsquoan Biota (Doushantuo Formation) an Ediacaranwindow on soft-bodied and multicellular microorganisms

John A Cunningham12 Kelly Vargas1 Zongjun Yin3 Stefan Bengtson2 ampPhilip C J Donoghue11 School of Earth Sciences University of Bristol Life Sciences Building 24 Tyndall Avenue Bristol BS8 1TQ UK2 Department of Palaeobiology andNordic Center for Earth Evolution SwedishMuseum of Natural History 10405 StockholmSweden

3 State Key Laboratory of Palaeobiology and Stratigraphy Nanjing Institute of Geology and Palaeontology Chinese Academyof Sciences Nanjing 210008 ChinaKV 0000-0003-1320-4195 SB 0000-0003-0206-5791 PCJD 0000-0003-3116-7463

Correspondence JohnCunninghambristolacuk

Abstract The Wengrsquoan Biota is a fossil Konservat-Lagerstaumltte in South China that is c 570 ndash 609 myr old and provides anunparalleled snapshot of marine life during the interval in whichmolecular clocks estimate that animal clades were diversifyingIt yields fossils that are three-dimensionally preserved in calcium phosphate with cellular and sometimes subcellular fidelityThe biota includes candidates for the oldest animals in the fossil record including embryonic larval and adult forms We arguethat although the Wengrsquoan Biota includes forms that could be animals none can currently be assigned to this group withconfidence Nonetheless the biota offers a rare and valuable window on the evolution of multicellular and soft-bodiedorganisms in the prelude to the Cambrian radiation

Received 21 November 2016 revised 28 February 2017 accepted 1 March 2017

The origin and evolutionary assembly of animal body planscomprises one of the most formative episodes in the history oflife Animals are ecosystem engineers and their appearancefundamentally changed our planetrsquos ecology (Butterfield 2011a)Despite the importance of this evolutionary episode many aspectsof the timing and nature of the event remain poorly constrainedMolecular-clock analyses estimate that animals originated by theCryogenian and diversified through the Ediacaran (Peterson ampButterfield 2005 Erwin et al 2011 dos Reis et al 2015) but fossilevidence of animals from before the Cambrian is controversial(Erwin et al 2011 dos Reis et al 2015 Cunningham et al 2017)The Wengrsquoan Biota is one of the few Lagerstaumltten from the criticalinterval in which early animals are expected according to molecular-clock studies In this Ediacaran fossil assemblage organisms arephosphatized in cellular and even subcellular detail providing a rareglimpse of soft-bodied and multicellular life at this time Earlyresearch appeared to fulfil expectations of the presence ofmetazoanswith reports of embryonic (Xiao et al 1998) larval (Chen et al2000 2002) and adult (Xiao et al 2000 Chen et al 2002 2004 Yinet al 2015) animals from the Wengrsquoan deposit Howeversubsequent analyses have cast doubt on this view and there iscurrently much disagreement over these interpretations (Bailey et al2007a Huldtgren et al 2011 Bengtson et al 2012 L Chen et al2014 Xiao et al 2014a) Here we review the stratigraphic positiongeological age and environmental setting of the deposit and presentan overview of the biota and an assessment of the phylogeneticaffinities of the various taxa

Stratigraphy and age

The Wengrsquoan Biota occurs within the Ediacaran DoushantuoFormation (551 ndash 635 Ma Condon et al 2005) of south China(Fig 1) In addition to the phosphatized microfossils fromWengrsquoanthis formation has yielded silicified microfossils (Yin et al 2004)

and macrofossils that are preserved as 2D carbonaceous compres-sions including macro-algae (Xiao et al 2002) and the putativectenophore Eoandromeda (Tang et al 2008 2011) The WengrsquoanBiota itself is known from localities in Wengrsquoan County GuizhouProvince The Doushantuo Formation overlies the Marinoan glacialtillites of the Cryogenian Nantuo Formation that can be dated to635 Ma (Condon et al 2005) It is overlain by the EdiacaranDengying Formation which contains fossils of the classicalEdiacara macrobiota (Sun 1986 Xiao et al 2005 Z Chen et al2014) The base of the Dengying Formation can be dated to 551 Ma(Condon et al 2005) In Wengrsquoan the Doushantuo Formation iscomposed of five units that have been described in detail by Xiaoet al (2014b) and Yin et al (2015) The Wengrsquoan Biota occursmainly in Unit 4 the Upper Phosphorite Member but also in Unit5 Unit 4 is divided into 4A a black phosphorite and 4B a greydolomitic phosphorite (Dornbos et al 2006 Xiao et al 2014abYin et al 2015)

The age of the biota has been debated (Budd 2008 Erwin ampValentine 2013 Xiao et al 2014a Yin et al 2015) with argumentsfocusing on the correlation of two karstic surfaces one at the top ofUnit 3 and the other within Unit 5 (for detailed discussion ofDoushantuo correlation see Zhu et al (2007) Zhu et al (2013) andYang et al (2015)) If the lower surface is correlated to the c582 Ma Gaskiers glaciation (Condon et al 2005) then the biotawould be younger than 582 Ma However the lower surface may beolder (Yin et al 2015) and if the upper karstic surface correlates tothe Gaskiers glaciation (Xiao et al 2014a) then the biota would beolder than 582 Ma Direct radiometric dates for Unit 4 at Wengrsquoanhave been inconclusive giving PbndashPb isochron ages of 572 plusmn36 Ma for Unit 4A (Y Chen et al 2009) and 599 plusmn 4 Ma for Unit 4B(Barfod et al 2002) However a recent UndashPb date of 609 plusmn 5 Mafrom a tuff immediately above Unit 4 at Zhancunping in HubeiProvince (Zhou et al 2017) suggests that the Wengrsquoan biota isprobably older than 609 plusmn 5 Ma and probably older than the

copy 2017 The Author(s) This is an Open Access article distributed under the terms of the Creative Commons Attribution License (httpcreativecommonsorglicensesby30) Published by The Geological Society of London Publishing disclaimer wwwgeolsocorgukpub_ethics

Review Focus Journal of the Geological Society

Published online May 3 2017 httpsdoiorg101144jgs2016-142 | Vol 174 | 2017 | pp 793ndash802

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Gaskiers glaciation which cannot be related to the karst surface atthe top of Unit 3 if this date is correct Acritarchs identical to thosecontaining embryo-like fossils are found just above an ash banddated to 6325 plusmn 05 Ma in Doushantuo sections from the YangtzeGorges (Yin et al 2007) suggesting that these organisms couldhave existed at this time In summary the biota is probably olderthan the classical but enigmatic Ediacaran biota and considerablypredates the rich animal fossil record of the Cambrian Putativeanimals from the assemblage are therefore candidates for the oldestanimals in the fossil record

Depositional environment preservation and reworking

The Wengrsquoan Biota is interpreted as having been deposited in anouter-shelf environment on a SE-facing passive margin (Jiang et al2011) Abundant wave ripples and cross-bedding features indicatedeposition above fair-weather wave base (Xiao amp Knoll 1999) The

fossils were probably deposited in oxic conditions (Shields et al2004) although phosphatization may have occurred in anoxicsediments (Muscente et al 2014 Schiffbauer et al 2014) The soft-bodied organisms of the biota are three-dimensionally preserved incalcium phosphate and can be preserved at a subcellular level(Hagadorn et al 2006 Huldtgren et al 2011) However even thebest-preserved specimens are a complex amalgam of cementsmaking it challenging to determine which aspects representpreserved biology (Xiao et al 2000 Bengtson 2003 Bengtson ampBudd 2004 Cunningham et al 2012a Schiffbauer et al 2012) Thepreservation of Wengrsquoan fossils is discussed in Box 1 The fossilsoccur either as or within phosphatic grains that have been abradedand rounded indicating transport from other parts of the basin afterinitial preservation (Xiao et al 2007b) In unit 4A a c 5 m thickblack phosphorite the fossils occur in reworked phosphatic clastsAs a result they cannot be released by acetic acid maceration andhave generally been studied in petrographic thin sections (eg Chen

Fig 1 The location and geologicalsetting of the Wengrsquoan Biota (a) Map ofChina showing the location of Wengrsquoan(b) Geological map of the Wengrsquoan area(c) Stratigraphic column of theBeidoushan section in the Wengrsquoan areaindicating Units 1 ndash 4 of the DoushantuoFormation the occurrence of the WengrsquoanBiota and the radiometric age constraintsdiscussed in the text Modified from Yinet al (2015)

Box 1 Preservation of Wengan fossils

The Wengrsquoan organisms like all exceptionally preserved soft-bodied remains were subjected to both post-mortem decay and later diagenetic and geologicalprocesses (Donoghue amp Purnell 2009) These processes alter the morphology of the fossils in ways that can be unpredictable Palaeontologists must take these factorsinto account rather than simply comparing the fossils with extant or freshly dead modern organisms This is particularly true given the simple nature of the biologicalstructures relevant to the interpretation of the Wengrsquoan Biota In the case of decay carefully designed experiments can help constrain which features can feasibly bepreserved elucidate likely preservation pathways and identify biases introduced by the decay process (Sansom 2014) Experiments have shown that animal embryoshave a relatively high preservation potential particularly when enclosed in a fertilization envelope whereas primary larvae have an extremely low likelihood of beingpreserved (Raff et al 2006 Gostling et al 2008 2009) In addition these experiments have identified the likely mechanism for Doushantuo-type preservation 3Dreplication of cells by robust bacterial pseudomorphs followed by phosphate mineralization (Raff et al 2008) The diagenetic and subsequent geological processesthat the fossil is subjected to can introduce artefacts (eg through crystal nucleation and growth) that have no connection to the original anatomy These processes aredifficult to simulate experimentally because of the timescales involved An alternative approach is to characterize the mineral phases that preserve biological anatomyv geological artefacts This has been carried out in fossils where there is agreement regarding affinity and anatomy and has allowed textural and chemical criteria tobe established and then applied to more contentious Wengrsquoan material (Cunningham et al 2012a 2014) In particular geological artefacts tend to have largereuhedral crystals with a preferred orientation higher X-ray attenuation and characteristic void-filling textures Geological artifacts typically also have high relativeabundances of P Ca and F and low abundances of C and S Failure to consider these processes andor the 3D nature of the specimens can lead to misinterpretations ofthe fossils as discussed in Box 2

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et al 2004 L Chen et al 2014 see Box 2 for a comparison of 2Dand 3D analytical techniques) In unit 4B a c 10 m thick greydolomitic phosphorite the microfossils are abundant and in placesare so concentrated that the layers resemble oolites This is agrainstone composed largely of microfossils that have beenphosphatized before being reworked transported and winnowed(Xiao ampKnoll 1999 Xiao et al 2007b) The fossils can be extractedby dissolution of the carbonate constituents of rock samples in weakacetic acid and manual sorting of the resulting residues Specimenscan then be studied using scanning electron microscopy (eg Xiaoet al 1998) or tomographic techniques (eg Hagadorn et al 2006)and can be re-embedded in resin and sectioned for furtherpetrographic and geochemical analyses (reviewed by Cunninghamet al 2014)

Overview of the Wengrsquoan Biota

Algae

A variety of algal taxa have been reported from Wengrsquoan (Zhao1986 Zhang 1989 Zhang amp Yuan 1992 Xiao et al 1998 2004Xiao 2004) Some simpler forms such as Archaeophycus (Fig 2j)show interesting similarities to extant bangialean red algae (Xiaoet al 1998) although other affinities cannot be ruled out (Xiao et al2014a) More complex forms such as Thallophyca and Parameciashare characters with floridophyte red algae including pseudopar-enchymous construction differentiated thalli and possible repro-ductive structures (Xiao et al 2004) However the putative algaehave received relatively little attention because of the focus on thesearch for animals Many specimens lack the overall form of aphotosynthetic organism For example the blades typical of variousseaweeds have not been recovered and it is hard to envisage howcells positioned centrally within globular masses would havefunctioned in a photosynthetic organism (Fig 3a and b) Algae mayhave been used as a wastebasket taxon for assorted irregular formsand rejected animal candidates These fossils merit further study andthere is a prospect that they may include developmental stages ofother organisms including the embryo-like fossils especially giventheir typically larger size

Acritarchs

The acritarchs (Fig 2k) from Wengrsquoan have been reviewedcomprehensively by Xiao et al (2014b) and form part of theDoushantuondashPertatataka microbiota (Zhou et al 2001 2007 Liuet al 2014) The phylogenetic affinities of acritarchs are unknownand they probably represent a polyphyletic assortment of eukaryotes(Huntley et al 2006) Some Doushantuo acritarchs contain embryo-like fossils (Yin et al 2007) leading to the suggestion that otherEdiacaran acritarchs might be resting cysts of these organisms(Cohen et al 2009) The interpretation of the DoushantuondashPertatataka acritarchs is therefore at least partially linked to that ofthe embryo-like fossils although they may well represent apolyphyletic assemblage The affinities of taxa should beconsidered on a case-by-case basis

Embryo-like fossils

Wengrsquoan fossils that have been interpreted as the embryos of earlyanimals (Xiao et al 1998) have been the focus of most attention anddebate (Fig 2andashf ) They have been interpreted as metazoans (Xiaoet al 1998) including bilaterians (Chen amp Chi 2005 J Chen et al2006 2009ab Yin et al 2013) as stem-group metazoans(Hagadorn et al 2006 Schiffbauer et al 2012 L Chen et al2014) or as members of non-metazoan clades (Bailey et al 2007abButterfield 2011b Huldtgren et al 2011 2012 L Chen et al 2014Zhang amp Pratt 2014) We consider the various claims below

Giant sulphur bacteria

Bailey et al (2007ab) proposed an interesting hypothesis that theembryo-like fossils might be giant sulphur bacteria similar to theliving Thiomargarita These bacteria can be similar in size andshape to the embryo-like fossils from Wengrsquoan and are capable ofundergoing at least a few rounds of palintomic division Howeversubsequent analyses have shown that these bacteria cannot accountfor key morphological aspects of the fossils such as the presence ofornamented envelopes outer acritarch vesicles and probable lipidvesicles and nuclei (Donoghue 2007 Xiao et al 2007b Huldtgrenet al 2011 Cunningham et al 2012b) Moreover evidence fromexperimental taphonomy showed that Thiomargarita cells are notreplicated by biofilm-forming bacteria meaning that they do notform the stable bacterial pseudomorphs that are thought to be theprecursor to exceptional phosphatization (Cunningham et al2012b see Box 1)

Bilaterians or eumetazoans

Reports of embryonic bilaterians do not withstand scrutiny Someare based on identifications of cell geometries argued to be uniqueto bilaterians These include specimens purported to preserveendodermal cords (J Chen et al 2009b) polar lobes (J Chen et al2006 2009a Yin et al 2013) embryonic polarity (J Chen et al2009ab) and duet cleavage (J Chen et al 2009a) In each case thespecimens can be alternatively interpreted as examples of embryo-like fossils that have undergone taphonomic and diageneticprocesses (Huldtgren et al 2011 Cunningham et al 2012a)Specimens interpreted as possible bilaterian or cnidarian gastrulaeand larvae (Chen et al 2000 2002 Chen amp Chi 2005) are moreprobably deformed cysts filled with phosphatic cements (Xiao et al2000) The presence of meroblastic embryos (Yin et al 2016)would represent the long sought-after confirmation of the presenceof animal embryos A possible alternative interpretation of thesespecimens which are associated with a large population known toundergo asynchronous division (Hagadorn et al 2006) is that theyhave undergone unequal division It is currently difficult to testbetween these possible interpretations

Total group animals

The embryo-like fossils probably represent one taxon dividing froma single cell to thousands of cells (Fig 2andashf ) This taxon has been

Box 2 2D versus 3D analysis

TheWengrsquoan fossils have been subjected to a wide range of analytical techniques These include scanning electron microscopy (which provides very high resolutionimages of the exterior of the specimen) analysis of petrographic thin sections (which affords a single cross-section but destroys the remainder of the fossil) andtomographic approaches (which allow the specimen to be imaged in three dimensions) Analyses of specimens in petrographic sections have yielded importantinsights including features that have not been identified using other techniques such as the cell clusters preserved within lsquoMegaclonophycusrsquo-stage embryoids(L Chen et al 2014) However the 2D nature of the data can make it difficult to make inferences regarding the 3D anatomy of the fossil and caution must beexercised Reports of gastrulae (Chen et al 2000 2002) cnidarian larvae (Chen et al 2000 2002) and adult bilaterians (Chen et al 2004) probably result frommisinterpretations of deformed cysts which are abundant in the deposit that have been studied only in two dimensions (Xiao et al 2000 Bengtson 2003 Bengtson ampBudd 2004 Bengtson et al 2012)

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Fig 2 Scanning electron microscope images of fossils from the Wengrsquoan biota (andashf ) Tianzhushania specimens at various stages of division from a singlecell (a) to many hundreds of cells (f ) Swedish Museum of Natural History (SMNH) X 6449ndashSMNH X 6454 (g) Helicoforamina SMNH X 6455 (h)Spiralicellula (from Tang et al 2008) (i) Caveasphaera SMNH X 6456 ( j) Archaeophycus a putative red alga SMNH X 6457 (k) Mengeosphaera anacritarch SMNH X 6458 (l) Eocyathispongia a putative sponge Nanjing Institute of Palaeontology and Geology (NIGPAS) 161760 (from Yin et al2015) Scale bar (a) 320 microm (b) 265 microm (c) 265 microm (d) 200 microm (e) 245 microm (f ) 280 microm (g) 395 microm (h) 380 microm (i) 250 microm ( j) 255 microm (k) 130 microm(l) 415 microm

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Fig 3 Synchrotron radiation X-ray tomographic microscopy (SRXTM andashh) and light microscopy (indashk) images of Wengrsquoan fossils (a b) a possible algaSMNH X 6459 comparable with Paramecia (c d) a peanut-shaped fossil SMNH X 6460 (e f ) Sinocyclocyclicus SMNH X 5322 (g h) RamitubusSMNH X 5326 (indashk) Light microscopy images of putative algae from Wengrsquoan Scale bar (a b) 270 microm (c d) 280 microm (e f ) 180 microm (g h) 175 microm(i j) 140 microm (k) 115 microm

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named either Tianzhushania orMegasphaera according to differenttaxonomic interpretations (Yin et al 2004 Xiao et al 2014b)Tianzhushania is preferred here (see Box 3) These specimens wereinterpreted as animal embryos by Xiao et al (1998) based on thesimilar size and the presence of palintomic cell division Y-shapedjunctions between cells and an ornate enclosing envelope Morerecently these have been considered as stem rather than crownanimals because later stages lack evidence for epithelial organiza-tion which is characteristic of modern embryos (Hagadorn et al2006) However the placement of these fossils in the animal total-group has also been questioned (Bailey et al 2007a Butterfield2011b Huldtgren et al 2011 L Chen et al 2014 Zhang amp Pratt2014)

None of the characters that have been used to justify an animalinterpretation are exclusive to animals (see Fig 4) Features such aspalintomic cleavage Y-shaped cell junctions and an ornateenvelope are found in non-animal groups (Huldtgren et al 20112012) They are therefore consistent with an animal interpretationbut they are not diagnostic characters They are insufficient either inisolation or in combination to justify an animal affinity

It has also been suggested that Tianzhushania exhibits charactersgained in the animal stem lineage L Chen et al (2014) describeddiscrete clusters of cells (lsquomatryoshkasrsquo) within embryo-like fossilswith hundreds of cells They interpreted these as reproductivepropagules and presented them as evidence for spatial celldifferentiation germndashsoma separation and apoptosis Based onthese characters along with functional cell adhesion obligatemulticellularity and the potential lack of a rigid cell wall L Chenet al (2014) argued that Tianzhushaniamight be a stem-animal thathad gained some but not all of the characters that are present inanimals but not choanoflagellates The occurrence of dividing cellswithin the embryo-like fossils is merely an expectation of theexisting observation that they exhibit asynchronous cell division(Hagadorn et al 2006) Nevertheless the interpretation ofdifferentiation and germndashsoma separation requires that the clustersare part of the embryo-like organism rather than an exogenousparasite L Chen et al (2014) suggested that there is adevelopmental continuation from the typical cells of these speci-mens and the clusters which rules out an exogenous originHowever there is a discontinuity between monads dyads and

Box 3 Taxonomy of the embryo-like fossils

The embryo-like fossils have been described under various genus and species names that are now considered to be different developmental stages or taphonomicvariants of a single taxon (Huldtgren et al 2011 Cunningham et al 2012a L Chen et al 2014 Xiao et al 2014ab) The names Megasphaera (single-celledspecimens) Parapandorina (multiple polyhedral cells) andMegaclonophycus (large numbers of usually spheroidal cells) are nowwidely considered to be synonyms(eg Huldtgren et al 2011 Cunningham et al 2012a Xiao et al 2014ab) However because of different taxonomic interpretations different researchers havereferred to this taxon as eitherMegasphaera (eg L Chen et al 2014 Xiao et al 2014ab) or Tianzhushania (eg Yin et al 2004 Huldtgren et al 2011 Cunninghamet al 2012a) The genus Tianzhushania and its type species T spinosa were described in 1978 for acanthomorphic acritarchs with cylindrical processes that wereknown from thin sections (Yin amp Li 1978) Yin et al (2001) subsequently described T tuberifera based on specimens with both cylindrical processes and sculpturedornament Megasphaera with the type species M inornata was described in 1986 for smooth envelopes (Chen amp Liu 1986) and later expanded by Xiao amp Knoll(2000) to accommodate specimens with sculptured envelopes (M ornata) Yin et al (2004) showed thatM ornata specimens when viewed in thin sections could besurrounded by an outer wall identical to that of Tianzhushania They therefore argued that T tuberifera which had been studied in thin sections was the same speciesas M ornata which had mainly been studied in specimens isolated from acid residues Yin et al (2004) proposed Tianzhushania ornata as the valid name for thistaxon As the various embryo-like stages can be found inside these specimens Huldtgren et al (2011) argued that Tianzhushania is the senior synonym ofMegasphaera Parapandorina andMegaclonophycus Xiao et al (2014ab) noted that the diagnosis of Tianzhushania had never been formally emended to includespecimens with sculptured envelopes They therefore proposed to retainMegasphaera for smooth or sculptured specimens that lack processes and Tianzhushania forspecimens that have smooth envelopes and processes The new genus Yinitianzhushania (basionym T tuberifera) was erected to accommodate those specimens thathave sculptured envelopes and cylindrical processes However this classification differentiatesMegasphaera from the other genera based on the absence of tubularprocesses which probably results from taphonomic loss rather than a biological difference We also find it unsatisfactory to place specimens from acid residues intoYinitianzhushania if they have a sculptured envelope and Tianzhushania if they do not This would result in a specimen with a sculptured envelope and tubularprocesses being placed in one genus (Yinitianzhushania) if it had lost only its processes and another (Tianzhushania) if it had also lost its sculptured envelope It istherefore preferable to place all of these taxa in a single genus Tianzhushania which we consider to be the senior synonym of Yinitianzhushania as well as ofMegasphaera Parapandorina and Megaclonophycus despite the fact that the diagnosis of Tianzhushania has not yet been formally revised to include specimenswith sculptured envelopes

Fig 4 Schematic representation ofeukaryote phylogeny modified afterRensing (2016) showing the distributionof characters relevant to the interpretationof the embryo-like fossil TianzhushaniaHere multicellularity includes bothaggregative multicellularity (eg slimemoulds) and clonal multicellularity(animals plants fungi various algae) aswell as both facultative (egchoanoflagellates) and obligatemulticellularity

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tetrads which show evidence for palintomy and larger lsquomatry-oshkarsquo clusters which do not (Tang 2015 Cunningham et al 2016)Although there must be a switch from palintomy at some point(Chen et al 2017) the lack of intermediates weakens the evidencefor an endogenous origin (Tang 2015 Cunningham et al 2016)

The argument for apoptosis is that because the enclosingenvelope imposes a constant volume throughout ontogeny the onlyway to create the space required for the putative reproductivestructures to grow is for other cells to die off However the volumeof Tianzhushaniamaywell not be constrained in this way given thatearly stages often do not occupy the full envelope and putative laterstages provide evidence for distension and then rupture of theenvelope (Liu et al 2009 Huldtgren et al 2011) The evidence fordifferentiation germndashsoma separation and programmed cell death istherefore unconvincing Moreover there is also uncertaintyregarding the other proposed animal characters There is noevidence that the walls of Tianzhushania are any less rigid thanthose of non-animal groups such as non-metazoan holozoans(Marshall amp Berbee 2011) amoebozoans (Olive 1975) ciliates(Park et al 2005) or volvocalean algae (Hallmann 2006) which alsohave Y-shaped cell junctions Nor is there evidence that celladhesion is different from that seen in groups such as non-metazoanholozoans (volvocalean algae achieve adhesion through cytoplas-mic bridges which are absent in the fossils)

To summarize Tianzhushania does not exhibit characters that aresufficient to identify it as an animal Evidence for the presence ofcharacters gained in the animal stem lineage is equivocal There istherefore no justification for an interpretation of Tianzhushania as ananimal although a stem-animal affinity cannot be definitively rejectedon the basis of current data (Huldtgren et al 2011 2012) Above allthe available evidence does not yet allow these fossils to be used tosubstantiate hypotheses on the timing of animal diversification

Other possibilities

A number of alternative interpretations have been proposed yet theaffinities of these organisms remain uncertain Comparisonswith non-metazoanholozoans (Huldtgren et al2011) algae (Butterfield 2011bLChen et al2014 ZhangampPratt 2014) orciliates are plausible but asyet unsubstantiated and require further investigation The primaryfactor that has hindered interpretation of these fossils is poorunderstanding of the later stages of the organismsrsquo ontogeny Anumber of candidates have been proposed but none are widelyacceptedXiao et al (2007a) suggested that helically coiled specimens(Fig 2g) now named Helicoforamina might be later stages perhapsrepresenting a coiled vermiform animal However this taxon isenigmatic and has also been argued to be an embryo of the ctenophore-like fossil Eoandromeda which has eight spiral arms (Tang et al2008 2011) or a single-celled stage of Spiralicellula (Fig 2h) a formthat resembles Tianzhushania but differs in having coiled cells(Huldtgren et al 2011) Peanut-shaped specimens with hundreds ofthousands of cells (Fig 3c and d) have also been interpreted as laterdevelopmental stages (Huldtgren et al 2011) These have single cellsand clusters of cells that are isolated from the main mass of cells andhave been argued to be reproductive propagules L Chen et al (2014)have also described specimens with putative reproductive propagulesIf Tianzhushania does reproduce via propagules then this indicates alifecycle incompatible with at least crown animals However in bothcases the interpretation as propagules has proven contentious (Xiaoet al 2012 Tang 2015) with a key issue being the incompleteknowledge of the lifecycle of Tianzhushania

Sponge-like fossils

Structures from the Wengrsquoan Biota have been interpreted assiliceous sponge spicules (Li et al 1998) However these have beenshown by subsequent analysis not to be composed of silica and to

lack convincing sponge characters (Zhang et al 1998 Antcliffeet al 2014 Muscente et al 2015) More recently Eocyathispongia(Fig 3c) has been described as a possible sponge from Wengrsquoan(Yin et al 2015) This is known from a single specimen that ispreserved at a cellular level Eocyathispongia is considered to beone of the strongest candidates for a Precambrian sponge Howeveralthough it could be a sponge it has no convincing spongeapomorphies such as pores or spicules just a generalized spongegestalt More detailed characterization of the anatomy ofEocyathispongia is required For example high-resolution tomog-raphy might reveal evidence for the presence or absence of spongecharacters and help to constrain the affinity of this enigmaticorganism

Tubular microfossils

A group of tubular microfossils assigned to the generaSinocyclocyclicus (Fig 3e and f) Ramitubus (Fig 3g and h)Crassitubus and Quadratitubus have been interpreted as cnidarian-like eumetazoans from the Wengrsquoan Biota (Xiao et al 2000 Chenet al 2002 Liu et al 2008) These genera have regularly spacedcross walls and have been compared with tabulate corals In a coral-like body plan the spaces between the cross walls represent theformer living positions of the polyp and would be expected to beempty or filled with diagenetic cements However the fossilspreserve biological structures in these spaces which is incompatiblewith a cnidarian interpretation (Cunningham et al 2015) There isno evidence to support a placement of these tubular fossils withineumetazoans or animals

Vernanimalcula

Vernanimalcula has been described from thin sections as aminiature adult bilaterian from the Wengrsquoan Biota (Chen et al2004 Petryshyn et al 2013) It is purported to preserve bilateriancharacters such as a mouth gut anus and paired coelomic cavitiesHowever all of the putative bilaterian characters can be alternativelyinterpreted as artefacts resulting from abiological diagenetic apatitecements which are ubiquitous in the deposit (Bengtson 2003Bengtson amp Budd 2004 Bengtson et al 2012 Cunningham et al2012a) Moreover 3D analyses show that Wengrsquoan fossils such asacritarchs and fertilization envelopes that clearly lack bilateralsymmetry can exhibit Vernanimalcula-like morphology whensectioned in particular orientations (Bengtson et al 2012) Thereis no evidential basis for interpreting Vernanimalcula either as abilaterian or as an animal of any kind

Summary and prospects

Research into the Wengrsquoan Biota is currently in a transitional phaseEarly research involved many attempts to demonstrate the long-expected presence of animals including bilaterians in theEdiacaran This has been followed by a spell of critical analysisof these claims that has shown that none of these fossils can so far beconfidently identified as stem- or crown-group metazoans Theresearch is now entering a phase where more targeted analysis of thepalaeobiology of each taxon is helping to constrain wide-ranginghypotheses of affinity more rigorously Many fossils are knownonly from a few specimens and have received limited attention Onesuch example is the enigmatic fossil Caveasphaera (Fig 2i) whichhas been tentatively compared with cnidarian embryos (Xiao ampKnoll 2000) but requires further investigation Such taxa betray acryptic diversity that has been overlooked because of the focus onTianzhushania

The Ediacaran was a critical interval in the history of life(Butterfield 2007) and the Wengrsquoan Biota offers a unique glimpseof microscopic multicellular and soft-bodied organisms at this time

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It can provide important insights into Ediacaran biology and theevolution of multicellular organisms at this time possibly includinganimal-type multicellularity Future work constraining the diversityaffinity and ontogeny of theWengrsquoan organisms is necessary beforethis potential is fully realized

Acknowledgements We thank S Dornbos and an anonymous referee forconstructive comments that helped improve the paper Data statement There areno data associated with this paper

Funding This work was funded by the Natural Environment ResearchCouncil (NEJ0183251 NEF00348X1 NEP0136781) the National NaturalScience Foundation of China (41672013) the Science Without Borders Program(CNPq Brazil) the Danish National Research Foundation (DNRF53) theSwedish Research Council (2010-3929 2013-4290) the Leverhulme Trust andthe Royal Society (Wolfson Merit Award and Newton Advanced Fellowship)

Scientific editing by Graham Shields-Zhou

ReferencesAntcliffe JB Callow RHT amp Brasier MD 2014 Giving the early fossil

record of sponges a squeeze Biological Reviews 89 972ndash1004 httpsdoiorg101111brv12090

Bailey JV Joye SB Kalanetra KM Flood BE amp Corsetti FA 2007aEvidence of giant sulphur bacteria in Neoproterozoic phosphorites Nature445 198ndash201 httpsdoiorg101038nature05457

Bailey JV Joye SB Kalanetra KM Flood BE amp Corsetti FA 2007bUndressing and redressing Ediacaran embryos ndash Reply Nature 446E10ndashE11 httpsdoiorg101038nature05754

Barfod GH Albarede F Knoll AH Xiao SH Telouk P Frei R amp BakerJ 2002 New LundashHf and PbndashPb age constraints on the earliest animal fossilsEarth and Planetary Science Letters 201 203ndash212 httpsdoiorg101016S0012-821X(02)00687-8

Bengtson S 2003 Tracing metazoan roots in the fossil record In Legakis ASfenthourakis S Polymeni R amp Thessalou-Legaki M (eds) The NewPanorama of Animal Evolution Proceedings of the 18th InternationalCongress of Zoology Pensoft Sofia 289ndash300

Bengtson S amp Budd G 2004 Comment on ldquoSmall bilaterian fossils from 40 to55 million years before the Cambrianrdquo Science 306 1291a httpsdoiorg101126science1101338

Bengtson S Cunningham JA Yin C amp Donoghue PCJ 2012 A mercifuldeath for the ldquoearliest bilaterianrdquo Vernanimalcula Evolution amp Development14 421ndash427 httpsdoiorg101111j1525-142X201200562x

Budd GE 2008 The earliest fossil record of the animals and its significancePhilosophical Transactions of the Royal Society of London Series B 3631425ndash1434 httpsdoiorg101098rstb20072232

Butterfield NJ 2007 Macroevolution and macroecology through deep timePalaeontology 50 41ndash55 httpsdoiorg101111j1475-4983200600613x

Butterfield NJ 2011a Animals and the invention of the Phanerozoic Earthsystem Trends in Ecology amp Evolution 26 81ndash87 httpsdoiorg101016JTree201011012

Butterfield NJ 2011b Terminal developments in Ediacaran embryologyScience 334 1655ndash1656 httpsdoiorg101126science1216125

Chen J amp Chi H 2005 Precambrian phosphatized embryos and larvae from theDoushantuo Formation and their affinities Guizhou (SW China) ChineseScience Bulletin 50 2193ndash2200 httpsdoiorg101360982004-727

Chen J Oliveri P et al 2000 Precambrian animal diversity Putativephosphatized embryos from the Doushantuo formation of ChinaProceedings of the National Academy of Sciences of the USA 974457ndash4462 httpsdoiorg101073pnas9794457

Chen J Oliveri P Gao F Dornbos SQ Li C Bottjer DJ amp Davidson EH 2002 Precambrian animal life Probable developmental and adult cnidarianforms from southwest China Developmental Biology 248 182ndash196 httpsdoiorg101006dbio20020714

Chen J Bottjer DJ et al 2004 Small bilaterian fossils from 40 to 55 millionyears before the Cambrian Science 305 218ndash222 httpsdoiorg101126science1099213

Chen J Bottjer DJ et al 2006 Phosphatized polar lobe-forming embryos fromthe Precambrian of southwest China Science 312 1644ndash1646 httpsdoiorg31257801644[pii]101126science1125964

Chen J Bottjer DJ et al 2009a Phase contrast synchrotron X-raymicrotomography of Ediacaran (Doushantuo) metazoan microfossilsPhylogenetic diversity and evolutionary implications PrecambrianResearch 173 191ndash200 httpsdoiorg101016jprecamres200904004

Chen J Bottjer DJ et al 2009b Complex embryos displaying bilateriancharacters from Precambrian Doushantuo phosphate deposits WengrsquoanGuizhou China Proceedings of the National Academy of Sciences of the USA106 19056ndash19060 httpsdoiorg101073pnas0904805106

Chen L Xiao S Pang K Zhou C amp Yuan X 2014 Cell differentiation andgermndashsoma separation in Ediacaran animal embryo-like fossils Nature 516238ndash241 httpsdoiorg101038nature13766

Chen L Xiao S Pang K Zhou C amp Yuan X 2017 Are the new EdiacaranDoushantuo embryo-like fossils early metazoans Reply Palaeoworld 25132ndash134 httpsdoiorg101016jpalwor201506005

Chen M amp Liu K 1986 The geological significance of newly discoveredmicrofossils from the Upper Sinian (Doushantuo Age) phosphorites ScientiaGeologica Sinica 46ndash55

Chen Y Jiang S Ling H amp Yang J 2009 PbndashPb dating of black shales fromthe Lower Cambrian and Neoproterozoic strata South China Chemie derErde 69 183ndash189 httpsdoiorg101016jchemer200812005

Chen Z Zhou C Xiao S Wang W Guan C Hua H amp Yuan X 2014New Ediacara fossils preserved in marine limestone and their ecologicalimplications Scientific Reports 4 4180 httpsdoiorg101038srep04180

Cohen PA Knoll AH amp Kodner RB 2009 Large spinose microfossils inEdiacaran rocks as resting stages of early animals Proceedings of the NationalAcademy of Sciences of the USA 106 6519ndash6524 httpsdoiorg101073pnas0902322106

Condon D Zhu M Bowring S Wang W Yang A amp Jin Y 2005 UndashPbages from the Neoproterozoic Doushantuo Formation China Science 30895ndash98 httpsdoiorg101126science1107765

Cunningham JA Thomas C-W et al 2012a Distinguishing geology frombiology in the Ediacaran Doushantuo biota relaxes constraints on the timing ofthe origins of bilaterians Proceedings of the Royal Society of London SeriesB 1737 2369ndash2376 httpsdoiorg101098rspb20112280

Cunningham JA Thomas C-W et al 2012b Experimental taphonomy ofgiant sulphur bacteria implications for the interpretation of the embryo-likeEdiacaran Doushantuo fossils Proceedings of the Royal Society of LondonSeries B 1734 1857ndash1864 httpsdoiorg101098rspb20112064

Cunningham JA Donoghue PCJ amp Bengtson S 2014 Distinguishingbiology from geology in soft-tissue preservation In Laflamme MSchiffbauer JD amp Darroch SAF (eds) Reading and Writing of the FossilRecord Preservational Pathways to Exceptional FossilizationPaleontological Society Papers 20 275ndash287

Cunningham JA Vargas K et al 2015 Critical appraisal of tubular putativemetazoans from the Ediacaran Wengrsquoan Dushantuo biota Proceedings of theRoyal Society of London Series B 282 20151169 httpsdoiorg01098rspb20151169

Cunningham JA Vargas K Marone F Bengtson S amp Donoghue PCJ2016 A multicellular organism with embedded cell clusters from theEdiacaran Wengrsquoan biota (Doushantuo Formation South China) Evolution ampDevelopment 18 308ndash316 httpsdoiorg101111ede12210

Cunningham JA Liu AG Bengtson S amp Donoghue PCJ 2017 The originof animals Can molecular clocks and the fossil record be reconciledBioEssays 39 201600120 httpsdoiorg101002bies201600120

Donoghue PCJ 2007 Palaeontology embryonic identity crisis Nature 445155ndash156 httpsdoiorgnature05520[pii]101038nature05520

Donoghue PCJ amp Purnell MA 2009 Distinguishing heat from light in debateover controversial fossils BioEssays 31 178ndash189 httpsdoiorg101002bies200800128

Dornbos SQ Bottjer DJ Chen J Gao F Oliveri P amp Li C 2006Environmental controls on the taphonomy of phosphatized animals andanimal embryos from the Neoproterozoic Doushantuo formation SouthwestChina Palaios 21 3ndash14 httpsdoiorg102110palo2004p04-37

dos Reis M Thawornwattana Y Angelis K Telford MJ Donoghue PCJamp Yang Z 2015 Uncertainty in the timing of origin of animals and the limitsof precision in molecular timescales Current Biology 25 2939ndash2950 httpsdoiorg101016jcub201509066

Erwin DH amp Valentine JW 2013 The Cambrian explosion the constructionof animal biodiversity Roberts amp Company Colorado

Erwin DH Laflamme M Tweedt SM Sperling EA Pisani D amp PetersonKJ 2011 The Cambrian conundrum early divergence and later ecologicalsuccess in the early history of animals Science 334 1091ndash1097 httpsdoiorg101126science1206375

Gostling NJ Thomas CW et al 2008 Deciphering the fossil record of earlybilaterian embryonic development in light of experimental taphonomyEvolution amp Development 10 339ndash349 httpdoiorg101111j1525-142X200800242x

Gostling NJ Dong XP amp Donoghue PCJ 2009 Ontogeny and taphonomyan experimental taphonomy study of the development of the brine shrimpArtemia salina Palaeontology 52 169ndash186 httpsdoiorg101111j1475-4983200800834x

Hagadorn JW Xiao S et al 2006 Cellular and subcellular structure ofNeoproterozoic animal embryos Science 314 291ndash294 httpsdoiorg101126science1133129

Hallmann A 2006 Morphogenesis in the family Volvocaceae Different tacticsfor turning an embryo right-side out Protist 157 445ndash461 httpsdoiorg101016jprotis200605010

Huldtgren T Cunningham JA Yin C Stampanoni M Marone FDonoghue PCJ amp Bengtson S 2011 Fossilized nuclei and germinationstructures identify Ediacaran lsquoanimal embryosrsquo as encysting protists Science334 1696ndash1699 httpsdoiorg101126science1209537

Huldtgren T Cunningham JA Yin CY Stampanoni M Marone FDonoghue PCJ amp Bengtson S 2012 Response to Comment on ldquoFossilizednuclei and germination structures identify Ediacaran lsquoanimal embryosrsquo asencysting protistsrdquo Science 335 1169 httpsdoiorg101126science1219076

800 J A Cunningham et al

by guest on November 10 2020httpjgslyellcollectionorgDownloaded from

Huntley JW Xiao S amp Kowalewski M 2006 13 Billion years of acritarchhistory An empirical morphospace approach Precambrian Research 14452ndash68

Jiang G Shi X Zhang S Wang Y amp Xiao S 2011 Stratigraphy andpaleogeography of the Ediacaran Doushantuo Formation (ca 635ndash551 Ma) inSouth China Gondwana Research 19 831ndash849 httpsdoiorg101016jgr201101006

Li C Chen J amp Hua T 1998 Precambrian sponges with cellular structuresScience 279 879ndash882 httpsdoiorg101126science2795352879

Liu P Xiao S Yin C Zhou C Gao L amp Tang F 2008 Systematicdescription and phylogenetic affinity of tubular microfossils from theEdiacaran Doushantuo Formation at Wengrsquoan South China Palaeontology51 339ndash366 httpsdoiorg101111j1475-4983200800762x

Liu P Yin C Chen S Tang F amp Gao L 2009 New data of phosphatizedglobular fossils from Wengrsquoan biota in the Ediacaran Doushantuo Formationand the problem concerning their affinity Acta Geoscientica Sinica 30457ndash464

Liu P Xiao S Yin C Chen S Zhou C amp Li M 2014 Ediacaranacanthorphic acritarchs and other microfossils from chert nodules of the upperDoushantuo Formation in the Yangtze Gorges area south ChinaPaleontology Memoir 72 1ndash139 httpsdoiorg10166613-009

Marshall WL amp Berbee ML 2011 Facing unknowns living cultures (Pirumgemmata gen nov sp nov and Abeoforma whisleri gen nov sp nov) frominvertebrate digestive tracts represent an undescribed clade within theunicellular opisthokont lineage Ichthyosporea (Mesomycetozoea) Protist162 33ndash57 httpsdoiorg101016jprotis201006002

Muscente AD Hawkins AD amp Xiao S 2014 Fossil preservation throughphosphatization and silicification in the Ediacaran Doushantuo Formation(South China) a comparative synthesis Palaeogeography PalaeoclimatologyPalaeoecology httpsdoiorg101016jpalaeo201410013

Muscente AD Michel FM Dale JG ampXiao S 2015 Assessing the veracityof Precambrian lsquospongersquo fossils using in situ nanoscale analytical techniquesPrecambrian Research 263 142ndash156 httpsdoiorg101016jprecamres201503010

Olive LS 1975 The Mycetozoans Academic Press New YorkPark KH Park JK Lee J amp Choi KS 2005 Use of molecular markers

for species identification of Korean Perkinsus sp isolated fromManila clams Ruditapes philippinarum Diseases of Aquatic Organisms 66255ndash263

Peterson KJ amp Butterfield NJ 2005 Origin of the Eumetazoa testingecological predictions of molecular clocks against the Proterozoic fossilrecord Proceedings of the National Academy of Sciences of the USA 1029547ndash9552 httpsdoiorg101073pnas0503660102

Petryshyn VA Bottjer DJ Chen J amp Gao F 2013 Petrographic analysis ofnew specimens of the putative microfossil Vernanimalcula guizhouena(Doushantuo Formation South China) Precambrian Research 225 58ndash66httpsdoiorg101016jprecamres201108003

Raff EC Villinski JT Turner FR Donoghue PCJ amp Raff RA 2006Experimental taphonomy shows the feasibility of fossil embryos Proceedingsof the National Academy of Sciences of the USA 103 5846ndash5851 httpsdoiorg101073Pnas0601536103

Raff EC Schollaert KL et al 2008 Embryo fossilization is a biologicalprocess mediated bymicrobial biofilms Proceedings of the National Academyof Sciences of the USA 105 19360ndash19365 httpsdoiorg101073Pnas0810106105

Rensing SA 2016 (Why) does evolution favour embryogenesis Trends inPlant Science 21 562ndash573 httpsdoiorg101016jtplants201602004

Sansom RS 2014 Experimental decay of soft tissues In Laflamme MSchiffbauer JD amp Darroch SAF (eds) Reading and Writing of the FossilRecord Preservational Pathways to Exceptional FossilizationPaleontological Society Papers 20 259ndash274

Schiffbauer JD Xiao S Sen Sharma K amp Wang G 2012 The origin ofintracellular structures in Ediacaran metazoan embryos Geology 40223ndash226 httpsdoiorg101130G325461

Schiffbauer JD Wallace AF Broce J amp Xiao S 2014 Exceptional fossilconservation through phosphatization In Laflamme M Schiffbauer JD ampDarroch SAF (eds) Reading and Writing of the Fossil RecordPreservational Pathways to Exceptional Fossilization PaleontologicalSociety Papers 20 59ndash82

Shields G Kimura H Yang J amp Gammon P 2004 Sulphur isotopicevolution of NeoproterozoicndashCambrian seawater new francolite-boundsulphate δ34S data and a critical appraisal of the existing record ChemicalGeology 204 163ndash182 httpsdoiorg101016jchemgeo200312001

Sun W 1986 Late Precambrian pennatulids (sea pens) from the eastern YangtzeGorge China Paracharnia gen nov Precambrian Research 31 361ndash375httpsdoiorg1010160301-9268(86)90040-9

Tang BL 2015 Are the new Ediacaran Doushantuo Megasphaera-likeacritarchs early metazoans Palaeoworld 25 128ndash131 httpsdoiorg101016jpalwor201506005

Tang F Yin C Bengtson S Liu P Wang Z amp Gao L 2008 Octoradiatespiral organisms in the Ediacaran of South China Acta Geologica SinicaEnglish Edition 82 27ndash34 httpsdoiorg101111j1755-67242008tb00321x

Tang F Bengtson S Wang Y Wang X amp Yin C 2011 Eoandromeda andthe origin of Ctenophora Evolution amp Development 13 408ndash414 httpsdoiorg101111J1525-142x201100499X

Xiao S 2004 New multicellular algal fossils and acritarchs in Doushantuo chertnodules (Neoproterozoic Yangtze Gorges south China) Journal ofPaleontology 78 393ndash401 httpsdoiorg1016660022-3360(2004)078lt0393NMAFAAgt20CO2

Xiao S amp Knoll AH 1999 Fossil preservation in the NeoproterozoicDoushantuo phosphorite Lagerstatte South China Lethaia 32 219ndash240httpsdoiorg101111j1502-39311999tb00541x

Xiao S amp Knoll AH 2000 Phosphatized animal embryos from theNeoproterozoic Doushantuo Formation at Wengrsquoan Guizhou South ChinaJournal of Paleontology 74 767ndash788 httpsdoiorg1016660022-3360(2000)074lt0767PAEFTNlt20CO2

Xiao S Zhang Y amp Knoll AH 1998 Three-dimensional preservation of algaeand animal embryos in a Neoproterozoic phosphorite Nature 391 553ndash558httpsdoiorg10103835318

Xiao S Yuan X amp Knoll AH 2000 Eumetazoan fossils in terminalProterozoic phosphorites Proceedings of the National Academy of Sciencesof the USA 97 13684ndash13689 httpsdoiorg101073pnas250491697

Xiao S Yuan X Steiner M amp Knoll AH 2002 Macroscopic carbonaceouscompressions in a terminal Proterozoic shale a systematic reassessment of theMiaohe biota south China Journal of Paleontology 76 347ndash376 httpsdoiorg1016660022-3360(2002)076lt0347MCCIATgt20CO2

Xiao S Knoll AH Yuan X amp Pueschel CM 2004 Phosphatizedmulticellular algae in the Neoproterozoic Doushantuo Formation Chinaand the early evolution of florideophyte red algae American Journal ofBotany 91 214ndash227 httpsdoiorg103732ajb912214

Xiao S Shen B Zhou C Xie G amp Yuan X 2005 A uniquely preservedEdiacaran fossil with direct evidence for a quilted bodyplan Proceedings ofthe National Academy of Sciences of the USA 102 10227ndash10232 httpsdoiorg101073pnas0502176102

Xiao S Hagadorn JW Zhou C amp Yuan X 2007a Rare helical spheroidalfossils from the Doushantuo Lagerstatte Ediacaran animal embryos come ofage Geology 35 115ndash118 httpsdoiorg101130G23277A1

Xiao S Zhou C amp Yuan X 2007b Undressing and redressing Ediacaranembryos Nature 446 E9ndashE10 httpsdoiorg101038nature05753

Xiao S Knoll AH Schiffbauer JD Zhou C amp Yuan X 2012 Comment onldquoFossilized nuclei and germination structures identify Ediacaran lsquoanimalembryosrsquo as encysting protistsrdquo Science 335 httpsdoiorg101126science1218814

Xiao S Muscente AD et al 2014a The Wengrsquoan biota and the Ediacaranradiation of multicellular eukaryotes National Science Review 1 498ndash520httpsdoiorg101093nsrnwu061

Xiao S Zhou C Liu PJ Wang D amp Yuan X 2014b Phosphatizedacanthomorphic acritarchs and related microfossils from the EdiacaranDoushantuo Formation at Wengrsquoan (South China) and their implications forbiostratigraphic correlation Journal of Paleontology 88 1ndash67 httpsdoiorg10166612-157R

Yang A Zhu M Zhang J Zhao F amp Luuml M 2015 Sequence stratigraphicsubdivision and correlation of the Ediacaran (Sinian) Doushantuo Formationof Yangtze Plate South China Journal of Palaeogeography 17 1ndash20 httpsdoiorg107605gdlxb201501001

Yin C Gao L amp Xing Y 2001 Discovery of Tianzhushania in Doushantuophosphorites in Wengrsquoan Guizhou Province Acta Palaeontologica Sinica40 497ndash504

Yin C Bengtson S amp Yue Z 2004 Silicified and phosphatizedTianzhushania spheroidal microfossils of possible animal originfrom the Neoproterozoic of South China Acta Palaeontologica Polonica49 1ndash12

Yin L amp Li Z 1978 Precambrian microfloras of southwest Chinawith referenceto their stratigraphic significanceMemoirs of the Nanjing Institute of Geologyand Palaeontology Academia Sinica 10 41ndash108

Yin L Zhu M Knoll AH Yuan X Zhang J amp Hu J 2007 Doushantuoembryos preserved inside diapause egg cysts Nature 446 661ndash663 httpsdoiorg101038nature05682

Yin Z Zhu M Tafforeau P Chen J Liu P amp Li G 2013 Earlyembryogenesis of potential bilaterian animals with polar lobe formation fromthe Ediacaran Wengrsquoan Biota South China Precambrian Research 22544ndash57 httpsdoiorg101016jprecamres201108011

Yin Z Zhu M Davidson EH Bottjer DJ Zhao F amp Tafforeau P 2015Sponge grade body fossil with cellular resolution dating 60 Myr before theCambrian Proceedings of the National Academy of Sciences of the USA 112E1453ndashE1460 httpsdoiorg101073pnas1414577112

Yin Z Zhu M Bottjer DJ Zhao F amp Tafforeau P 2016 Meroblasticcleavage identifies some Ediacaran Doushantuo (China) embryo-like fossils asmetazoans Geology G382621 httpsdoiorg101130G382621

Zhang X amp Pratt BR 2014 Possible algal origin and life cycle of EdiacaranDoushantuo microfossils with dextral spiral structure Journal ofPaleontology 88 92ndash98 httpsdoiorg10166613-014

Zhang Y 1989 Multicellular thallophytes with differentiated tissues from LateProterozoic phosphate rocks of South China Lethaia 22 113ndash132 httpsdoiorg101111j1502-39311989tb01674x

801Fossils of the Ediacaran Wengrsquoan Biota

by guest on November 10 2020httpjgslyellcollectionorgDownloaded from

Zhang Y amp Yuan X 1992 New data on multicellular thallophytes and fragmentsof cellular tissues from Late Proterozoic phosphate rocks South China Lethaia25 1ndash18 httpsdoiorg101111j1502-39311992tb01788x

Zhang Y Yuan X amp Yin L 1998 Interpreting late Precambrian microfossilsScience 282 1783 httpsdoiorg101126science28253951783a

Zhao D 1986 The discovery of phosphatic red algae in the Sinian DoushantuoFormation Acta Sedimentologica Sinica 4 126ndash127

ZhouC BrasierMDampXueY 2001 Three-dimensional phosphatic preservationof giant acritarchs from the Terminal Proterozoic Doushantuo Formation inGuizhou and Hubei provinces south China Palaeontology 44 1157ndash1178httpsdoiorg1011111475-498300219

Zhou C Xie G McFadden K Xiao S amp Yuan X 2007 The diversificationand extinction of DoushantuondashPertatataka acritarchs in South China

causes and biostratigraphic significance Geological Journal 42 229ndash262httpsdoiorg101002gj1062

Zhou C Li X Xiao S Lan Z Ouyang Q Guan C amp Chen Z 2017 A newSIMS zircon UndashPb date from the Ediacaran Doushantuo Formation ageconstraint on the Wengrsquoan biota Geological Magazine httpsdoiorg101017S0016756816001175

Zhu M Zhang J amp Yang A 2007 Integrated Ediacaran (Sinian)chronostratigraphy of South China Palaeogeography PalaeoclimatologyPalaeoecology 254 7ndash61 httpsdoiorg101016jpalaeo200703025

Zhu M Lu M et al 2013 Carbon isotope chemostratigraphy and sedimentaryfacies evolution of the Ediacaran Doushantuo Formation in western HubeiSouth China Precambrian Research 225 7ndash28 httpsdoiorg101016jprecamres201107019

802 J A Cunningham et al

by guest on November 10 2020httpjgslyellcollectionorgDownloaded from