Discovery of the oldest bilaterian from the Ediacaranof South AustraliaScott D. Evansa,1,2, Ian V. Hughesb, James G. Gehlingc

, and Mary L. Drosera

aDepartment of Earth Sciences, University of California, Riverside, CA 92521; bSection of Ecology, Behavior and Evolution, Division of Biological Sciences,University of California San Diego, La Jolla, CA 92093; and cDepartment of Palaeontology, South Australia Museum, Adelaide, SA 5000, Australia

Edited by Neil H. Shubin, University of Chicago, Chicago, IL, and approved February 17, 2020 (received for review January 21, 2020)

Analysis of modern animals and Ediacaran trace fossils predictsthat the oldest bilaterians were simple and small. Such organismswould be difficult to recognize in the fossil record, but should havebeen part of the Ediacara Biota, the earliest preserved macro-scopic, complex animal communities. Here, we describe Ikariawariootia gen. et sp. nov. from the EdiacaraMember, South Australia,a small, simple organism with anterior/posterior differentiation.We find that the size and morphology of Ikaria match predictionsfor the progenitor of the trace fossil Helminthoidichnites—indica-tive of mobility and sediment displacement. In the Ediacara Member,Helminthoidichnites occurs stratigraphically below classic Ediacarabody fossils. Together, these suggest that Ikaria represents one ofthe oldest total group bilaterians identified from South Australia,with little deviation from the characters predicted for their last com-mon ancestor. Further, these trace fossils persist into the Phanerozoic,providing a critical link between Ediacaran and Cambrian animals.

bilaterian | Ediacaran | Ediacara Biota | phylogenetics | trace fossil

The first macroscopic animal fossils are recognized within thesoft-bodied Ediacara Biota (1, 2). Among these are candi-

date poriferans (3), cnidarians (4), and ctenophores (5). RareEdiacaran taxa have been interpreted as putative bilaterians,namely, Kimberella (6, 7). However, small furrowed trace fossilsare generally accepted as definitive evidence for total groupbilaterians in the Ediacaran (8–10). The size and morphology ofthese trace fossils suggest that they were produced by millimeter-scale organisms that would be difficult to recognize in the fossilrecord (11).Helminthoidichnites are horizontal trace fossils found in Edia-

caran and Phanerozoic deposits globally (12, 13). Helminthoi-dichnites is a curvilinear burrow that can be preserved on bothbed tops as well as bottoms and occurs most commonly on thebase of thin (submillimeter to millimeter scale) discontinuoussand bodies, or shims (8, 14). The preservation of Helminthoi-dichnites in negative relief flanked by positive levees on bedbottoms indicates that the progenitor moved under thin sandbodies following deposition and burial, displacing sediment (8,9, 11, 14). Observed relationships between intersecting Hel-minthoidichnites indicates the ability of the progenitor to movevertically, albeit on millimeter scales (11). Rare Helminthoidichnitespenetrating body fossils of macroscopic taxa may represent theoldest evidence of scavenging (11).In modern environments, Helminthoidichnites-type structures

can be produced by a variety of bilaterians (9, 11). A likely pro-genitor for Ediacaran Helminthoidichnites has yet to be identified,although it has been suggested that these were produced by simple“worm-like animals” (9). Critically, based on the nature of sedi-ment displacement by a horizontally burrowing organism, it wouldhave been small, with a maximum diameter less than that observedfor Helminthoidichnites. Such behavior necessitates anterior–pos-terior differentiation, as well as a coelom, consistent with bilaterian-grade tissue organization (8, 9, 11, 15).Helminthoidichnites are preserved abundantly within the

Ediacara Member, Rawnsley Quartzite in the Flinders Rangesand surrounding regions of South Australia (16). The Ediacara

Member consists of shallow marine sandstone event beds 50 to500 m below a basal Cambrian disconformity (17). At the NationalHeritage Nilpena site, the excavation and reconstruction of 37-m-scale fossiliferous bed surfaces reveals in situ communities of theEdiacara Biota (18). At Nilpena, and sections within the FlindersRanges, Helminthoidichnites occurs more than 100 m below thefirst appearance of Kimberella (19, 20). There are currently noradiometric dates to constrain the absolute age of the EdiacaraMember; however, significant overlap of taxa with well-establisheddeposits from the White Sea region of Russia indicates that theseare likely between 560 and 551 million years old (21–24). A similarpattern of leveed, horizontal trace fossils (although in this caseassigned to the ichnogenus Archaeonassa) occurring strati-graphically below classic White Sea assemblage body fossils inRussia (9, 23) may corroborate the early appearance of tracefossils in South Australia.

ResultsHere, we report the discovery of the new genus, new speciesIkaria wariootia, the interpreted progenitor of Helminthoidichn-ites. We have identified 108 Ikaria on a single bed surface (1T-A)and 19 from float at multiple localities, preserved in negativehyporelief on the base of sandstone beds (Fig. 1). Ikaria is foundin fine-grained sandstones in two facies representing depositionin relatively shallow marine environments between fair-weatherand storm-wave base (14, 17, 25).

Significance

The transition from simple, microscopic forms to the abundanceof complex animal life that exists today is recorded within soft-bodied fossils of the Ediacara Biota (571 to 539 Ma). Perhapsmost critically is the first appearance of bilaterians—animalswith two openings and a through-gut—during this interval.Current understanding of the fossil record limits definitive evi-dence for Ediacaran bilaterians to trace fossils and enigmaticbody fossils. Here, we describe the fossil Ikaria wariootia, one ofthe oldest bilaterians identified from South Australia. This or-ganism is consistent with predictions based on modern animalphylogenetics that the last ancestor of all bilaterians was simpleand small and represents a rare link between the Ediacaran andthe subsequent record of animal life.

Author contributions: S.D.E., J.G.G., and M.L.D. designed research; S.D.E., I.V.H., and M.L.D.performed research; S.D.E., I.V.H., J.G.G., and M.L.D. analyzed data; and S.D.E., I.V.H.,J.G.G., and M.L.D. wrote the paper.

The authors declare no competing interest.

This article is a PNAS Direct Submission.

Published under the PNAS license.1Present address: Department of Paleobiology, Smithsonian Institution, Washington,DC 20560.

2To whom correspondence may be addressed. Email: EvansSD@si.edu.

This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2001045117/-/DCSupplemental.

First published March 23, 2020.

www.pnas.org/cgi/doi/10.1073/pnas.2001045117 PNAS | April 7, 2020 | vol. 117 | no. 14 | 7845–7850

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Systematic DescriptionIkaria wariootia gen. et sp. nov.

Etymology. The generic name is after the word “Ikara,” which is theAdnyamathanha name for Wilpena Pound, and means “meetingplace” in the Adnyamathanha language. Ikara is the major land-mark in view from Nilpena, and the fossil has been named toacknowledge the original custodians of the land; species arenamed for Warioota Creek, which runs from the Flinders Rangesto Nilpena Station.

Holotype. P57685 (Fig. 1; South Australia Museum).

Paratype. P57686 (Fig. 2A; South Australia Museum).

Field Paratypes. 1T-A bed 001 to 007 (Fig. 2 B–J; Nilpena).

Horizon and Locality. Ediacara Member, Rawnsley Quartzite atthe National Heritage Nilpena field site and Bathtub Creek.

Diagnosis. Irregular millimeter-scale ovoid preserved in negativehyporelief. The major axis length averages 2.3 times the minoraxis. There is distinct asymmetry along the major axis with oneend wider and more broadly curved (white star in Figs. 1C and 2D–F, G, and J). In profile, the broader end is preserved in moresignificant negative relief and with a steeper curvature (black starin Figs. 1D and 2 H and I). Rare specimens are bent about thelong axis (Fig. 2 F and J) and/or exhibit potential evidence ofmodularity, with two to five body divisions (Fig. 2 D and E).

Description. I. wariootia are well-defined elongate ovals, fusiformin shape (Figs. 1 and 2). Three-dimensional (3D) laser scansdemonstrate clear anterior/posterior differentiation, with oneend distinctly smaller and more tightly curved. Length of themajor axis ranges from 1.9 to 6.7 mm and the minor axis from 1.1to 2.4 mm. Preserved depth ranges from 0.6 to 1.6 mm. There is aconsistent linear relationship between total length and totalwidth (SI Appendix, Fig. S1A). The relationships between totallength and depth (SI Appendix, Fig. S1B) as well as width anddepth (SI Appendix, Fig. S2) are irregular. Depth is always lessthan width, suggesting that fossils of Ikaria are compressed. Thisconfirms previous interpretations that the preserved depth ofspecimens from the Ediacara Member is strongly influenced bytaphonomic processes (e.g., ref. 26).

While the morphology of Ikaria is very simple, it is consistentacross specimens and is unambiguously distinct from otherstructures. The consistent shape and length-to-width ratio arenot what is observed for rip-up clasts of organic mats, which areirregular (14). Although mat rip-ups are found within theEdiacara Member, they do not occur in the same lithologies andfacies as Ikaria (14, 25), which represent deposition in a lower-energy environment. Furthermore, rip-up clasts have a differentbiostratinomic and diagenetic history than Ikaria and all otherbody fossils (14). The outer margin of Ikaria is sharp, and theyare preserved with considerable relief, distinct from the sur-rounding matrix and organic mat textures (Fig. 2). This is con-sistent with other nonsessile taxa from the Ediacara Member(27), suggesting that Ikaria represents the body fossil of a free-living organism.Ikaria can be easily differentiated from other taxa preserved on

the same bed surface and of similar size and scale (SI Appendix,Fig. S3). Thus, it is unlikely a juvenile form of a previously de-scribed taxon. The lack of larger specimens with comparablemorphology suggests that maximum size is ∼7 mm. The recogni-tion of other taxa on the same surface preserved at the same scaleand with similarly well-defined outer margins distinct from theorganic mat corroborates the biologic, body-fossil origin of Ikaria.Specimens of Ikaria are found in association with Helmin-

thoidichnites, albeit rarely (Fig. 2A). The range of Ikaria widthsplots entirely within those measured for Helminthoidichnites withthe maximum size of body fossils not exceeding that of tracefossils (SI Appendix, Fig. S4). Further, the Anderson–Darling testindicates that size-frequency distributions are not significantlydifferent (P value 0.448). This, combined with clear anterior–posterior differentiation, suggests that Ikaria is the only knowncontemporaneous body fossil with the suite of characters pre-dicted for the progenitor of Helminthoidichnites.

DiscussionIn general, it is rare to have trace fossils and the organisms thatproduced them preserved together, particularly with respect to mo-bile metazoans. This can be attributed to both the different preser-vational pathways between body and trace fossils and the ability ofthe animal to move away from the area where it left evidence ofactivity (28, 29). In certain cases, the morphological characteristics ofbody fossils from the same deposits can be used to reliably determinethe progenitors of particular trace fossils (e.g., ref. 30).Body fossils in the Ediacara Member, including Ikaria, are well

preserved on the bottoms of centimeter-scale sandstone beds

A B DC

Fig. 1. Type specimen of I. wariootia from Nilpena, including (A) photograph; and (B–D) 3D laser scans. Notice distinct bilateral symmetry (wider endidentified by white star in C and deeper end by black star in D). P57685. (Scale bars, 1 mm.)

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B C

D E F

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I J

Fig. 2. Photographs (A and B) and 3D laser scans (C–J) of I. wariootia. (A) Specimen (white arrow) associated with Helminthoidchnites. (B–E) Associatedspecimens; black boxes in B and C are the same specimen shown in close up in negative hyporelief (D) and inverted (E). (F and J) Bent specimens. (G and H) Nbedding plane (G) and profile (H) of the same specimen. (I) Profile demonstrating variable relief. Notice correlation between broader, wider end (white stars)in the bedding-pane view and more significant relief end (black stars) in the profile. (A) P57686. (B–E ) 1T-A 001 to 003. (F ) 1T-A 004. (G and H) 1T-A 005. (I)1T-A 006. (J) 1T-A 007. (Scale bars, 1 mm.)

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with early mineralization of overlying sand casting the tops ofthese organisms following burial (8, 14, 16). Although counter-parts are identified in rare cases on bed tops, these are poorlypreserved and at a resolution that is unlikely to produce identi-fiable features at the same scale as Ikaria. In contrast, Helmin-thoidichnites is found on both bed tops and bottoms, but mostcommonly on the base of millimeter-thick shims, where wellpreserved body fossils are rare (8, 14). Negative hyporeliefpreservation indicates that Helminthoidichnites formed after thedeposition of overlying sand, with the organism that produced itcapable of moving into and out of thin layers of sand (11). Thispredicts that we should only find Helminthoidichnites and itsprogenitor on the same bed bottom in rare instances when it diedwhile burrowing underneath thin sand bodies. Given the simplemorphology and preservation of both body and trace fossil innegative relief, even if Ikaria was preserved at the end of a trail, itis unlikely that it would be possible to confidently identify asdistinct from that trace. We interpret the surprising discovery ofHelminthoidichnites with nearby Ikaria (Fig. 2A) as the result ofvertical movement from the bedding plane in the region betweenthe end of its trace fossil and its final resting place. While thisscenario was likely exceedingly rare, it may represent the onlysituation in which it would be possible to distinguish associatedbody and trace fossils and further corroborates interpretations ofIkaria as the progenitor of Helminthoidichnites.We propose that Ikaria is the trace maker of Helminthoi-

dichnites and potentially the oldest, definitive bilaterian, at leastas represented in the fossil record of South Australia. Kimberella,the only other taxon from the Ediacara Member that is consis-tently reconstructed as a bilaterian, occurs significantly higherstratigraphically than the earliest appearance of Helminthoi-dichnites (6, 7, 19, 20). Similarities between taxonomic assem-blages have been consistently cited as evidence that White Seaassemblage fossils from the Ediacara Member, including Kim-berella, are conservatively 560 to 551 Ma (21–24). The strati-graphic position of Helminthoidichnites suggests that the firstappearance of Ikaria was likely within this age range or possiblyearlier. Burrows initially interpreted to be from much olderEdiacaran rocks in Uruguay have uncertain age constraints (31,32). Trace fossils from Brazil, representing the activity ofmeiofaunal bilaterians, occur 30 to 40 m above a tuff dated at555 Ma and in close association with Cloudina, indicating thatthey are likely younger than Ikaria (10, 24). A recently describedsegmented bilaterian from South China, associated with tracefossils, is interpreted to be younger, larger, and more complexthan Ikaria (33).The ability to move and produce recognizable trace fossils is

not unique to bilaterians. Complex body and trace fossils fromolder Ediacaran deposits were probably produced by musculareumetazoans interpreted to be cnidarians (34). Dickinsonia, andsimilar Ediacara Biota fossils, likely do not represent crown-group bilaterians, but were mobile and left trace fossils (35,36). Modern protists generate simple burrows, but are typicallysmaller than Ikaria (37, 38). Laboratory experiments demon-strate that mobile foraminifera form burrows in clay and silt;however, they do not produce burrows in fine-grained or coarsersand (37). Large testate amoeba in deep-sea environments areassociated with horizontal trails similar to those observed in theEdiacaran, but these are surficial and represent movement byrolling (38). Flatworms are mobile, but do not burrow below thesediment–water interface and rarely leave trace fossils (39).Among these examples, expression on bed bottoms with furrowsis unique to Helminthoidichnites and suggests mobility associatedwith significant displacement of medium sand grains. This isconsistent with reconstructions of Ikaria containing musculatureand a coelom (15, 40). Combined with the relative size of bodyand trace fossils, these characteristics are unique to bilaterians.

Polarity of relief and curvature characterize anterior/posteriordifferentiation in Ikaria (Fig. 3), supported by directed move-ment in trace fossils. Preservation of v-shaped transverse ridgeswithin Helminthoidichnites suggests peristaltic mobility (ref. 11;Fig. 2A). Ikaria morphology implies a potentially modular bodyconstruction, which would have aided in muscular organizationrequired for peristalsis (40). Sediment displacement and scav-enging reveal that Ikaria likely had a coelom, mouth, anus, andthrough-gut (11, 15, 40), although these are unlikely to bereproduced in the fossil record. Preferential preservation ofHelminthoidichnites under thin sand bodies indicates that Ikariasought out these environments, possibly due to increased oxygenavailability (11, 14, 20). Ultimately, as the depth of overlying sandincreases, oxygenated environments give way to sulfidic, in-hospitable settings due to decomposition of organic matter, sup-ported by the restriction of Helminthoidichnites to beds <15 mmthick (11, 14, 20). Ikaria was likely able to detect organic matterburied in well-oxygenated environments as well as potentially toxicconditions, suggesting rudimentary sensory abilities. Combined,these features suggest that, despite the simple morphology that canbe directly observed in fossil specimens of Ikaria, this organism wasremarkably complex, compared with contemporaneous EdiacaraBiota taxa.Molecular phylogenetic analysis of modern metazoans dem-

onstrates that developmental programing is highly conservedbetween disparate groups. Initially, this led to hypotheses thatthe last common ancestor (LCA) of bilaterians (animals with twoopenings and a through-gut) was relatively complex, containingmany of the features common to a variety of such groups, in-cluding eyes, segmentation, appendages, and a heart (41–43).Expansion of this analysis to nonbilaterian animals and theirclosest single-celled ancestors instead indicates that componentsof these conserved developmental pathways have deep ancestry(see ref. 44 for discussion). Combined with recent evidence for asister-group relationship between Xenacoelamorpha and Bilateria,this suggests that the bilaterian LCA was a simple, small, mobileorganism with anterior/posterior differentiation and limitedsensory abilities (44–49). Remarkably, these predictions agreeclosely with the characters identified here for Ikaria.

Fig. 3. Reconstruction of Ikaria in life position forming a Helminthoidichnites-type trail.

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Recognition of the totality of traits in Ikaria is reliant on bothbody and associated trace fossils. Given the simple morphologyof Ikaria, it is unlikely that we would be able to confidently assignit to the Bilateria, or even Metazoa, without this relationship.This is consistent with hypotheses that the apparent gap betweenmolecular clock predictions for the early divergence of bilateriansand their later appearance in the fossil record is the result of theirpredicted simple morphology (44, 49). Thus, similar prephylum,total group bilaterians may be found elsewhere in the Precambrianfossil record; Ikaria provides a search image for the future iden-tification of such forms.The stratigraphic position of Helminthoidichnites suggests that

Ikaria is the oldest total group bilaterian from the fossil record ofSouth Australia. Ikaria represents a rare example in early animalevolution where phylogenetic predictions correspond directlywith the fossil record. Further, the global distribution and rec-ognition of Helminthoidichnites in Cambrian strata (12, 13) isdistinct from the overwhelming majority of the Ediacara Biota.While Ikaria is not necessarily responsible for the production ofall examples of Helminthoidichnites, it is likely that Ikaria and/orrelated taxa are rare fossil animals that existed across theEdiacaran–Cambrian boundary.

Materials and MethodsFossil specimens from the National Heritage fossil site at Nilpena remain inthe field due to occurrence on large (square-meter to square-decameterscale) bedding planes (18). These specimens are identified by bed and fieldnumbers (e.g., 1T-A 001). Float specimens from Nilpena are collected andhoused at the South Australia Museum in Adelaide and identified byP numbers.

Specimens of Ikaria and Helminthoidichnites were documented throughdigital photography, using a Pentax K-50 digital single-lens reflex, and latexmolds. Helminthoidichnites width was measured by using digital calipersdirectly on fossil specimens. Detailed morphological investigation was madepossible by 3D laser scans, collected by using the HDI Compact C506 3D laserscanner. The accuracy of this scan system is reported to 12 μm. Scans wereprocessed by using the FlexScan3D software. Measurements were conductedon 3D scans by using the FlexScan3D software. Screenshots of these scans arepresented in Figs. 1 and 2.

We used the Anderson–Darling test to statistically compare the size fre-quency distributions of Helminthoidichnites and Ikaria using the freelyavailable PAST software (https://folk.uio.no/ohammer/past/). For this analy-sis, we compared the average widths of 606 individual Helminthoidichniteswith the maximum widths of 112 Ikaria from Nilpena (Dataset S1). Thisanalysis produced a statistically significant P value (>0.05) of 0.448, in-dicating that we cannot reject the null hypothesis that the two samples aretaken from populations with equal distributions.

Data Availability Statement. All data discussed in this paper are available inDataset S1.

ACKNOWLEDGMENTS. This work was supported by NASA Exobiology Pro-gram Grant NNX14AJ86G (to M.L.D.) and NASA Earth and Space ScienceFellowship Program Grant NNXPLANET17F-0124 (to S.D.E.). S.D.E. and M.L.D.were supported by the NASA Astrobiology Institute under CooperativeAgreement NNA15BB03A, issued through the Science Mission Directorate.We thank R. and J. Fargher for access to the National Heritage NilpenaEdiacara fossil site on their property, acknowledging that this land lieswithin the Adnyamathanha Traditional Lands. Fieldwork was facilitatedby M. A. Binnie, M. Droser, R. Droser, M. Dzaugis, M. E. Dzaugis, P. Dzaugis,M. Ellis, C. Hall, E. Hughes, C. Peddie, J. Perry, D. Rice, R. Surprenant, andL. Tarhan. We thank D. Erwin and J. Irving for helpful discussion regardingthis manuscript. S. Wasif created Fig. 3.

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