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Discovery of the oldest bilaterian from the of South Australia

Scott D. Evansa,1,2, Ian V. Hughesb, James G. Gehlingc, and Mary L. Drosera

aDepartment of , University of California, Riverside, CA 92521; bSection of , Behavior and , 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 and Ediacaran trace predicts Member consists of shallow marine sandstone event beds 50 to that the oldest bilaterians were simple and small. Such 500 m below a basal disconformity (17). At the National would be difficult to recognize in the record, but should have Heritage Nilpena site, the excavation and reconstruction of 37-m- been part of the Ediacara Biota, the earliest preserved macro- scale fossiliferous bed surfaces reveals in situ communities of the Ikaria scopic, complex communities. Here, we describe Ediacara Biota (18). At Nilpena, and sections within the Flinders wariootia gen. et sp. nov. from the Ediacara Member, South Australia, Ranges, Helminthoidichnites occurs more than 100 m below the a small, simple with anterior/posterior differentiation. first appearance of (19, 20). There are currently no We find that the size and morphology of Ikaria match predictions radiometric dates to constrain the absolute age of the Ediacara for the progenitor of the Helminthoidichnites—indica- tive of mobility and sediment displacement. In the Ediacara Member, Member; however, significant overlap of taxa with well-established Helminthoidichnites occurs stratigraphically below classic Ediacara deposits from the White Sea region of Russia indicates that these – body fossils. Together, these suggest that Ikaria represents one of are likely between 560 and 551 million old (21 24). A similar the oldest total group bilaterians identified from South Australia, pattern of leveed, horizontal trace fossils (although in this case with little deviation from the characters predicted for their last com- assigned to the ichnogenus Archaeonassa) occurring strati- mon ancestor. Further, these trace fossils persist into the , graphically below classic White Sea assemblage body fossils in providing a critical link between Ediacaran and Cambrian animals. Russia (9, 23) may corroborate the early appearance of trace fossils in South Australia. bilaterian | Ediacaran | Ediacara Biota | phylogenetics | trace fossil Results he first macroscopic animal fossils are recognized within the Here, we report the discovery of the new genus, new species Tsoft-bodied Ediacara Biota (1, 2). Among these are candi- Ikaria wariootia, the interpreted progenitor of Helminthoidichn- date poriferans (3), cnidarians (4), and ctenophores (5). Rare ites. We have identified 108 Ikaria on a single bed surface (1T-A) Ediacaran taxa have been interpreted as putative bilaterians, and 19 from float at multiple localities, preserved in negative namely, Kimberella (6, 7). However, small furrowed trace fossils hyporelief on the base of sandstone beds (Fig. 1). Ikaria is found are generally accepted as definitive evidence for total group in fine-grained sandstones in two facies representing deposition EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES bilaterians in the Ediacaran (8–10). The size and morphology of in relatively shallow marine environments between fair-weather these trace fossils suggest that they were produced by millimeter- and storm-wave base (14, 17, 25). scale organisms that would be difficult to recognize in the fossil record (11). Significance 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 both The transition from simple, microscopic forms to the abundance bed tops as well as bottoms and occurs most commonly on the of complex animal life that exists today is recorded within soft- bodied fossils of the Ediacara Biota (571 to 539 Ma). Perhaps base of thin (submillimeter to millimeter scale) discontinuous most critically is the first appearance of bilaterians—animals sand bodies, or shims (8, 14). The preservation of Helminthoi- with two openings and a through-gut—during this interval. dichnites in negative relief flanked by positive levees on bed Current understanding of the fossil record limits definitive evi- bottoms indicates that the progenitor moved under thin sand dence for Ediacaran bilaterians to trace fossils and enigmatic bodies following deposition and burial, displacing sediment (8, body fossils. Here, we describe the fossil Ikaria wariootia, one of 9, 11, 14). Observed relationships between intersecting Hel- the oldest bilaterians identified from South Australia. This or- minthoidichnites indicates the ability of the progenitor to move Helminthoidichnites ganism is consistent with predictions based on modern animal vertically, albeit on millimeter scales (11). Rare phylogenetics that the last ancestor of all bilaterians was simple penetrating body fossils of macroscopic taxa may represent the and small and represents a rare link between the Ediacaran and oldest evidence of scavenging (11). the subsequent record of animal life. In modern environments, Helminthoidichnites-type structures

can be produced by a variety of bilaterians (9, 11). A likely pro- Author contributions: S.D.E., J.G.G., and M.L.D. designed research; S.D.E., I.V.H., and M.L.D. genitor for Ediacaran Helminthoidichnites has yet to be identified, performed research; S.D.E., I.V.H., J.G.G., and M.L.D. analyzed data; and S.D.E., I.V.H., although it has been suggested that these were produced by simple J.G.G., and M.L.D. wrote the paper. “worm-like animals” (9). Critically, based on the nature of sedi- The authors declare no competing interest. ment displacement by a horizontally burrowing organism, it would This article is a PNAS Direct Submission. have been small, with a maximum diameter less than that observed Published under the PNAS license. for Helminthoidichnites. Such behavior necessitates anterior–pos- 1Present address: Department of , Smithsonian Institution, Washington, terior differentiation, as well as a coelom, consistent with bilaterian- DC 20560. gradetissueorganization (8, 9, 11, 15). 2To whom correspondence may be addressed. Email: [email protected]. Helminthoidichnites are preserved abundantly within the This article contains supporting information online at https://www.pnas.org/lookup/suppl/ Ediacara Member, Rawnsley in the Flinders Ranges doi:10.1073/pnas.2001045117/-/DCSupplemental. and surrounding regions of South Australia (16). The Ediacara

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

Systematic Description While the morphology of Ikaria is very simple, it is consistent Ikaria wariootia gen. et sp. nov. across specimens and is unambiguously distinct from other structures. The consistent shape and length-to-width ratio are Etymology. The generic name is after the word “Ikara,” which is the not what is observed for rip-up clasts of organic mats, which are Adnyamathanha name for Wilpena Pound, and means “meeting irregular (14). Although mat rip-ups are found within the place” in the Adnyamathanha language. Ikara is the major land- Ediacara Member, they do not occur in the same lithologies and Ikaria mark in view from Nilpena, and the fossil has been named to facies as (14, 25), which represent deposition in a lower- acknowledge the original custodians of the land; species are energy environment. Furthermore, rip-up clasts have a different biostratinomic and diagenetic history than Ikaria and all other named for Warioota Creek, which runs from the Flinders Ranges Ikaria to Nilpena Station. body fossils (14). The outer margin of is sharp, and they are preserved with considerable relief, distinct from the sur- Holotype. P57685 (Fig. 1; South Australia Museum). rounding matrix and organic mat textures (Fig. 2). This is con- sistent with other nonsessile taxa from the Ediacara Member Ikaria Paratype. P57686 (Fig. 2A; South Australia Museum). (27), suggesting that represents the body fossil of a free- living organism. Field Paratypes. 1T-A bed 001 to 007 (Fig. 2 B–J; Nilpena). Ikaria can be easily differentiated from other taxa preserved on the same bed surface and of similar size and scale (SI Appendix, Horizon and Locality. Ediacara Member, Rawnsley Quartzite at Fig. S3). Thus, it is unlikely a juvenile form of a previously de- the National Heritage Nilpena field site and Bathtub Creek. scribed taxon. The lack of larger specimens with comparable morphology suggests that maximum size is ∼7 mm. The recogni- Diagnosis. Irregular millimeter-scale ovoid preserved in negative tion of other taxa on the same surface preserved at the same scale hyporelief. The major axis length averages 2.3 times the minor and with similarly well-defined outer margins distinct from the axis. There is distinct asymmetry along the major axis with one organic mat corroborates the biologic, body-fossil origin of Ikaria. end wider and more broadly curved (white star in Figs. 1C and 2 Specimens of Ikaria are found in association with Helmin- D–F, G, and J). In profile, the broader end is preserved in more thoidichnites, albeit rarely (Fig. 2A). The range of Ikaria widths Helminthoidichnites significant negative relief and with a steeper curvature (black star plots entirely within those measured for with in Figs. 1D and 2 H and I). Rare specimens are bent about the the maximum size of body fossils not exceeding that of trace SI Appendix – long axis (Fig. 2 F and J) and/or exhibit potential evidence of fossils ( , Fig. S4). Further, the Anderson Darling test modularity, with two to five body divisions (Fig. 2 D and E). indicates that size-frequency distributions are not significantly different (P value 0.448). This, combined with clear anterior– Ikaria Description. I. wariootia are well-defined elongate ovals, fusiform posterior differentiation, suggests that is the only known contemporaneous body fossil with the suite of characters pre- in shape (Figs. 1 and 2). Three-dimensional (3D) laser scans Helminthoidichnites. demonstrate clear anterior/posterior differentiation, with one dicted for the progenitor of end distinctly smaller and more tightly curved. Length of the Discussion major axis ranges from 1.9 to 6.7 mm and the minor axis from 1.1 In general, it is rare to have trace fossils and the organisms that to 2.4 mm. Preserved depth ranges from 0.6 to 1.6 mm. There is a produced them preserved together, particularly with respect to mo- consistent linear relationship between total length and total bile metazoans. This can be attributed to both the different preser- SI Appendix A width ( , Fig. S1 ). The relationships between total vational pathways between body and trace fossils and the ability of SI Appendix B length and depth ( , Fig. S1 ) as well as width and the animal to move away from the area where it left evidence of depth (SI Appendix, Fig. S2) are irregular. Depth is always less activity (28, 29). In certain cases, the morphological characteristics of than width, suggesting that fossils of Ikaria are compressed. This body fossils from the same deposits can be used to reliably determine confirms previous interpretations that the preserved depth of the progenitors of particular trace fossils (e.g., ref. 30). specimens from the Ediacara Member is strongly influenced by Body fossils in the Ediacara Member, including Ikaria, are well taphonomic processes (e.g., ref. 26). preserved on the bottoms of centimeter-scale sandstone beds

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G I J

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Fig. 2. Photographs (A and B) and 3D laser scans (C–J)ofI. wariootia.(A) Specimen (white arrow) associated with Helminthoidchnites.(B–E) Associated specimens; 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)N bedding 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.)

Evans et al. PNAS Latest Articles | 3of6 Downloaded by guest on September 27, 2021 with early mineralization of overlying sand casting the tops of these organisms following burial (8, 14, 16). Although counter- parts are identified in rare cases on bed tops, these are poorly preserved 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 most commonly on the base of millimeter-thick shims, where well preserved body fossils are rare (8, 14). Negative hyporelief preservation indicates that Helminthoidichnites formed after the deposition of overlying sand, with the organism that produced it capable of moving into and out of thin layers of sand (11). This predicts that we should only find Helminthoidichnites and its progenitor on the same bed bottom in rare instances when it died while burrowing underneath thin sand bodies. Given the simple morphology and preservation of both body and trace fossil in negative relief, even if Ikaria was preserved at the end of a trail, it is unlikely that it would be possible to confidently identify as distinct from that trace. We interpret the surprising discovery of Helminthoidichnites with nearby Ikaria (Fig. 2A) as the result of vertical movement from the bedding plane in the region between the end of its trace fossil and its final resting place. While this scenario was likely exceedingly rare, it may represent the only situation in which it would be possible to distinguish associated body and trace fossils and further corroborates interpretations of Ikaria as the progenitor of Helminthoidichnites. Fig. 3. Reconstruction of Ikaria in life position forming a Helminthoidichnites- We propose that Ikaria is the trace maker of Helminthoi- type trail. dichnites and potentially the oldest, definitive bilaterian, at least as represented in the fossil record of South Australia. Kimberella, Polarity of relief and curvature characterize anterior/posterior the only other taxon from the Ediacara Member that is consis- Ikaria tently reconstructed as a bilaterian, occurs significantly higher differentiation in (Fig. 3), supported by directed move- stratigraphically than the earliest appearance of Helminthoi- ment in trace fossils. Preservation of v-shaped transverse ridges dichnites within Helminthoidichnites suggests peristaltic mobility (ref. 11; (6, 7, 19, 20). Similarities between taxonomic assem- A Ikaria blages have been consistently cited as evidence that White Sea Fig. 2 ). morphology implies a potentially modular body assemblage fossils from the Ediacara Member, including Kim- construction, which would have aided in muscular organization berella, are conservatively 560 to 551 Ma (21–24). The strati- required for peristalsis (40). Sediment displacement and scav- Ikaria graphic position of Helminthoidichnites suggests that the first enging reveal that likely had a coelom, mouth, anus, and appearance of Ikaria was likely within this age range or possibly through-gut (11, 15, 40), although these are unlikely to be earlier. Burrows initially interpreted to be from much older reproduced in the fossil record. Preferential preservation of Helminthoidichnites Ikaria Ediacaran rocks in Uruguay have uncertain age constraints (31, under thin sand bodies indicates that 32). Trace fossils from Brazil, representing the activity of sought out these environments, possibly due to increased meiofaunal bilaterians, occur 30 to 40 m above a tuff dated at availability (11, 14, 20). Ultimately, as the depth of overlying sand 555 Ma and in close association with Cloudina, indicating that increases, oxygenated environments give way to sulfidic, in- they are likely younger than Ikaria (10, 24). A recently described hospitable settings due to of organic matter, sup- Helminthoidichnites < segmented bilaterian from South China, associated with trace ported by the restriction of to beds 15 mm Ikaria fossils, is interpreted to be younger, larger, and more complex thick (11, 14, 20). was likely able to detect organic matter than Ikaria (33). buried in well-oxygenated environments as well as potentially toxic The ability to move and produce recognizable trace fossils is conditions, suggesting rudimentary sensory abilities. Combined, not unique to bilaterians. Complex body and trace fossils from these features suggest that, despite the simple morphology that can older Ediacaran deposits were probably produced by muscular be directly observed in fossil specimens of Ikaria,thisorganismwas eumetazoans interpreted to be cnidarians (34). , and remarkably complex, compared with contemporaneous Ediacara similar Ediacara Biota fossils, likely do not represent crown- Biota taxa. group bilaterians, but were mobile and left trace fossils (35, Molecular phylogenetic analysis of modern metazoans dem- 36). Modern generate simple burrows, but are typically onstrates that developmental programing is highly conserved smaller than Ikaria (37, 38). Laboratory experiments demon- between disparate groups. Initially, this led to hypotheses that strate that mobile form burrows in clay and silt; the last common ancestor (LCA) of bilaterians (animals with two however, they do not produce burrows in fine-grained or coarser openings and a through-gut) was relatively complex, containing sand (37). Large testate amoeba in deep-sea environments are many of the features common to a variety of such groups, in- associated with horizontal trails similar to those observed in the cluding eyes, segmentation, appendages, and a heart (41–43). Ediacaran, but these are surficial and represent movement by Expansion of this analysis to nonbilaterian animals and their rolling (38). are mobile, but do not burrow below the closest single-celled ancestors instead indicates that components sediment–water interface and rarely leave trace fossils (39). of these conserved developmental pathways have deep ancestry Among these examples, expression on bed bottoms with furrows (see ref. 44 for discussion). Combined with recent evidence for a is unique to Helminthoidichnites and suggests mobility associated sister-group relationship between Xenacoelamorpha and , with significant displacement of medium sand grains. This is this suggests that the bilaterian LCA was a simple, small, mobile consistent with reconstructions of Ikaria containing musculature organism with anterior/posterior differentiation and limited and a coelom (15, 40). Combined with the relative size of body sensory abilities (44–49). Remarkably, these predictions agree and trace fossils, these characteristics are unique to bilaterians. closely with the characters identified here for Ikaria.

4of6 | www.pnas.org/cgi/doi/10.1073/pnas.2001045117 Evans et al. Downloaded by guest on September 27, 2021 Recognition of the totality of traits in Ikaria is reliant on both Specimens of Ikaria and Helminthoidichnites were documented through body and associated trace fossils. Given the simple morphology digital photography, using a Pentax K-50 digital single-lens reflex, and latex of Ikaria, it is unlikely that we would be able to confidently assign molds. Helminthoidichnites width was measured by using digital calipers it to the Bilateria, or even Metazoa, without this relationship. directly on fossil specimens. Detailed morphological investigation was made This is consistent with hypotheses that the apparent gap between possible by 3D laser scans, collected by using the HDI Compact C506 3D laser scanner. The accuracy of this scan system is reported to 12 μm. Scans were molecular clock predictions for the early divergence of bilaterians processed by using the FlexScan3D software. Measurements were conducted and their later appearance in the fossil record is the result of their on 3D scans by using the FlexScan3D software. Screenshots of these scans are predicted simple morphology (44, 49). Thus, similar prephylum, presented in Figs. 1 and 2. total group bilaterians may be found elsewhere in the We used the Anderson–Darling test to statistically compare the size fre- fossil record; Ikaria provides a search image for the future iden- quency distributions of Helminthoidichnites and Ikaria using the freely tification of such forms. available PAST software (https://folk.uio.no/ohammer/past/). For this analy- The stratigraphic position of Helminthoidichnites suggests that sis, we compared the average widths of 606 individual Helminthoidichnites Ikaria is the oldest total group bilaterian from the fossil record of with the maximum widths of 112 Ikaria from Nilpena (Dataset S1). This South Australia. Ikaria represents a rare example in early animal analysis produced a statistically significant P value (>0.05) of 0.448, in- evolution where phylogenetic predictions correspond directly dicating that we cannot reject the null hypothesis that the two samples are with the fossil record. Further, the global distribution and rec- taken from populations with equal distributions. ognition of Helminthoidichnites in Cambrian strata (12, 13) is distinct from the overwhelming majority of the Ediacara Biota. Data Availability Statement. All data discussed in this paper are available in Dataset S1. While Ikaria is not necessarily responsible for the production of Helminthoidichnites Ikaria all examples of , it is likely that and/or ACKNOWLEDGMENTS. This work was supported by NASA Exobiology Pro- related taxa are rare fossil animals that existed across the gram Grant NNX14AJ86G (to M.L.D.) and NASA Earth and Space Ediacaran–Cambrian boundary. Fellowship Program Grant NNXPLANET17F-0124 (to S.D.E.). S.D.E. and M.L.D. were supported by the NASA Institute under Cooperative Materials and Methods Agreement NNA15BB03A, issued through the Science Mission Directorate. We thank R. and J. Fargher for access to the National Heritage Nilpena Fossil specimens from the National Heritage fossil site at Nilpena remain in Ediacara fossil site on their property, acknowledging that this land lies the field due to occurrence on large (square-meter to square-decameter within the Adnyamathanha Traditional Lands. Fieldwork was facilitated scale) bedding planes (18). These specimens are identified by bed and field by M. A. Binnie, M. Droser, R. Droser, M. Dzaugis, M. E. Dzaugis, P. Dzaugis, numbers (e.g., 1T-A 001). Float specimens from Nilpena are collected and M. Ellis, C. Hall, E. Hughes, C. Peddie, J. Perry, D. Rice, R. Surprenant, and housed at the South Australia Museum in Adelaide and identified by

L. Tarhan. We thank D. Erwin and J. Irving for helpful discussion regarding DEVELOPMENTAL BIOLOGY P numbers. this manuscript. S. Wasif created Fig. 3.

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