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Discovery of the Oldest Bilaterian from the Ediacaran of South Australia

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Discovery of the Oldest Bilaterian from the Ediacaran of South Australia Discovery of the oldest bilaterian from the Ediacaran of South Australia Scott 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 predicts Member consists of shallow marine sandstone event beds 50 to that the oldest bilaterians were simple and small. Such organisms 500 m below a basal Cambrian disconformity (17). At the National would be difficult to recognize in the fossil 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 animal 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 organism with anterior/posterior differentiation. first appearance of Kimberella (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 trace fossil 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 years 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 Phanerozoic, 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 DEVELOPMENTAL BIOLOGY 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 Paleobiology, 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 Quartzite in the Flinders Ranges doi:10.1073/pnas.2001045117/-/DCSupplemental. and surrounding regions of South Australia (16). The Ediacara First published March 23, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2001045117 PNAS | April 7, 2020 | vol. 117 | no. 14 | 7845–7850 Downloaded by guest on September 29, 2021 A B C D 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.
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