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The advent of : The view from the SPECIAL FEATURE

Mary L. Drosera,1 and James G. Gehlingb,c

aDepartment of Sciences, University of California, Riverside, CA 92521; bSouth Museum, , SA 5000, Australia; and cUniversity of Adelaide, Adelaide, SA 5000, Australia

Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved December 9, 2014 (received for review April 15, 2014) Patterns of origination and of early complex on this relationships within the Ediacara Biota and, importantly, reveals the planet are largely interpreted from the of the Precam- morphologic disparity of these taxa. brian soft-bodied Ediacara Biota. These fossils occur globally and However, although fossils of the Ediacara Biota are not easily represent a diverse suite of living in marine environments. classified with modern taxa, they nonetheless provide the record Although these exceptionally preserved assemblages are typi- of early animals. One of the primary issues is that they are soft- cally difficult to reconcile with modern phyla, examination of the bodied and preserved in a manner that is, in many cases, unique to morphology, , and of these taxa provides keys to the Ediacaran. An alternative venue for providing insight into these their relationships with modern taxa. Within the more than 30 million organisms and the manner in which they fit into early evo- y range of the Ediacara Biota, fossils of these multicellular organisms lution is offered by examination of the , morphology, demonstrate the advent of mobility, heterotrophy by multicellular and taphonomy of fossils of the Ediacara Biota. In this article, we animals, skeletonization, sexual reproduction, and the assembly of review the framework of the fossils of the Ediacara Biota and dis- complex , all of which are attributes of modern animals. cuss some of the new evidence that demonstrates how these taxa fit This approach to these fossils, without the constraint of attempting into the record of early metazoan evolution without the constraints phylogenetic reconstructions, provides a mechanism for comparing of attempting phylogenetic reconstructions. these taxa with both living and extinct animals. The Temporal and Spatial Record Ediacara | animals | Ediacaran | | fossils Fossils of the Ediacara biota occur at 40 localities worldwide, with four particularly good localities; namely, southeastern New- ossils of the Ediacara Biota consisting of macroscopic, mor- foundland, the of South Australia, the White Sea Fphologically diverse and generally soft-bodied organisms (1) Region of , and (2, 16). The Ediacara fossil assem- occur globally in strata spanning 575–541 Mya, marking the end blages have traditionally been demarcated as three successive of the (2). The record of these organisms predates assemblages: the Avalon, the White Sea, and the Nama, which the well-known Explosion by nearly 40 million y and have been interpreted as a reflection of evolutionary controls, as provides critical information concerning evolutionary innovations evidenced by the radiometric ages of several key localities (2). in early complex multicellular life forms on Earth. However, their However, there are also strong secondary preservational (17, 18) phylogenetic affinities and their relationship to Cambrian shelly and paleoenvironmental controls (19, 20). EVOLUTION and nonbiomineralized biotas, and thus their overall place in an- What is apparent is that the older Avalon Assemblage contains imal evolution on this planet (1), remain poorly constrained. In- adistinctassemblageoftaxathatexhibitonlyafewbroadmor- deed, most are classified only to the and level. The phologic [e.g., and arboreomorphs (cf. 21)] types. apparent discontinuity between the Precambrian and the Cam- Particularly striking are the common -like self-similar brian fossil record is largely based on the absence of skeletal hard branching forms with surface area/volume ratios, parts until the very end of the Ediacaran period and the lack of which are comparable to modern osmotrophic . Although Cambrian-type constructional morphologies among the Ediacara this feeding type is restricted to these bacteria in the modern , – biota. With rare exceptions (3 6), fossils of the Ediacara biota are these self-similar growths may have represented a strategy for EARTH, ATMOSPHERIC,

not found in Cambrian strata, and those that are reported are not overcoming physiologic constraints that typically make osmo- AND PLANETARY SCIENCES typical Ediacara morphologies. For lack of a strong alternative, trophy prohibitive for macroscopic life forms (22). Further, these much of the biota is, thus, commonly interpreted to have gone extinct by the end of the Ediacaran period (2, 7). A few Ediacaran Significance fossils have been interpreted as stem group metazoans, but the Cambrian period marks the unequivocal appearance of most Patterns of evolution, origination, and of early - major phyla. mal life on this planet are largely interpreted from fossils of the Historically, the majority of Ediacara fossils were interpreted soft-bodied Ediacara Biota, Earth’s earliest multicellular com- as members of modern animal phyla. Radially symmetrical and munities preserved globally. The record of these organisms sea-pen-like forms have generally been assigned to the , predates the well-known by nearly 40 and segmented forms with generally bilateral symmetry have been million and provides critical information concerning early associated with and (e.g., refs. 8 and 9). How- experimentation with complex life-forms on Earth. Here we ever, the challenges of finding unequivocal morphologic characters show that, although in appearance, these organisms look very linking the majority of these fossils to modern phyla, as well as their strange and unfamiliar, many of them may have had a unusual style of preservation as casts and molds in medium-grained and/or ecology similar to animals today, and some were most , prompted suggestions of a wide range of alternative certainly bilaterians, cnidarians, and poriferans. phylogenetic affinities, ranging from an extinct of “Ven- dobionts” (10) to prokaryotic colonies (11), (12), Author contributions: M.L.D. and J.G.G. designed research; M.L.D. and J.G.G. performed (13), and fungi (14). The lack of forms with clear morphologic ties to research; M.L.D. analyzed data; and M.L.D. and J.G.G. wrote the paper. even Cambrian further complicates this issue. Lacking clear The authors declare no conflict of interest. relationships to modern taxa, recently, a novel classification of these This article is a PNAS Direct Submission. taxa based on morphologic similarities and differences among just 1To whom correspondence should be addressed. Email: [email protected] the Ediacara fossils has led to the interpretation of at least six, and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. possibly nine, (1, 15). This provides testable hypotheses for 1073/pnas.1403669112/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1403669112 PNAS | April 21, 2015 | vol. 112 | no. 16 | 4865–4870 Downloaded by guest on October 2, 2021 early unusual and distinct macroorganisms may have been im- a distinctive role in Ediacara seafloor ecology, both as members of portant in cycling dissolved organic that may have been Ediacara communities and likely as preservational mediators (17). abundant in the Ediacaran times (22). Although TOS are known from Avalon fossil assemblages (33), Elements of the Avalon Assemblage persisted (19, 21), but they achieved unprecedented abundance, morphologic diversity, there are major increases in biologic and ecologic complexity and complexity as part of the second wave radiation (32). Many of following in the wake of the appearance of the older Avalon As- the new body and taxa characteristic of second wave semblage that more strongly relate to animals as we understand assemblages occur in intimate association with TOS and appear to them. The younger, “second wave” of the Ediacara Biota com- represent matground-based, heterotrophic lifestyles. prising the White Sea and Nama assemblages includes a wide range of new taxa (Fig. 1) (2, 21) that exhibit pronounced biologic Environments of the Ediacara Biota and ecologic innovation, as evidenced by dramatic increases in There are abundant data and general consensus that all the body plans and ecospace use; it is a radiation in its own right. deposits that Ediacara fossils are marine in origin (19, 34). Notable aspects of this radiation include dramatic increases in Although a terrestrial origin was recently proposed (35), this mobility (18); the appearance of undisputed bilaterians, such as hypothesis has been rigorously tested and is not consistent with burrowing organisms and stem-group mollusks (e.g., refs. 23 and any of the sedimentologic data (31, 34, 36–40). Fossils of the 24); the advent of sexual reproduction (25); the appearance of the Ediacara Biota are indeed preserved in a variety of marine first biomineralizers (26, 27); and the advent of active heterotro- environments (2), from outer shelf and slope settings in volcanic phy by multicellular organisms (24, 28–30, 31). sediments of forearc basins of the Avalon Terrane (41, 42) to Moreover, this diversification in macrofauna body plans and prograding carbonate platforms such as southern (43, 44) was accompanied by a diversification in organically and shallow marine prograding siliciclastic environments of the bound microbial substrates (microbial mats) recorded in the form (19, 20, 45, 46). events enabled of extensive sedimentary textures both physically and biologically samples of benthic communities to be conserved that included mediated. These textured organic surfaces (TOS) are diverse sessile body fossils and trace fossils. However, these snapshots patterned assemblages of structures that partially or completely also include elements of the of each surface, beginning cover bedding surfaces. Lacking autonomous taxonomic traits, with recruitment of benthic taxa (18, 25), ambient currents and they nonetheless possess discrete, repeating characters (11, 32). wave events, ecologic succession (47), degradation of organisms, The constituent organisms may have been members of a pro- and evidence of current deformation and loss of sessile frondous karyotic, microbial . However, it is likely that they were forms in the final burial event (48, 49). eukaryotic forms (32) and that certain large and multicomponent Within each Ediacaran assemblage there are considerable TOS may actually consist of assemblages of multicellular body differences in the biotic composition, depending on wave energy, fossils (25, 32). Regardless of phylogenetic affinity, TOS played the sedimentary substrate, and the depth of benthic communities

Fig. 1. Common Ediacara biota fossils from the Ediacara Member, Rawnsley , Flinders Ranges, South Australia. (A) costata with pre- contraction outline. (B) dorothea preserved as body casts and external molds where casts have been lost. (C) Two specimens of minchami.(D) quadrata.(E) Multilayered sandstone case of Bradgatia sp. (F) Sandstone cast of scratch traces, Kimberichnus teruzzii, produced by K. quadrata.(G) floundersi.(H) Internal cast of three walls of simplex.(I) Helminthoidichnites isp., groove and levee traces preserved on a bed base. Specimens D and G are from the Ediacara Conservation Park; other specimens are from the Nilpena Heritage Site. (Scale bar: 1 cm.)

4866 | www.pnas.org/cgi/doi/10.1073/pnas.1403669112 Droser and Gehling Downloaded by guest on October 2, 2021 (19, 20). As a consequence, the most useful field exposures are in shallow marine settings between fair-weather and storm wave those in which whole bedding surfaces can be exposed and base. The rich fossil assemblages of this wave-base sand SPECIAL FEATURE studied from differing paleoenvironmental settings within a re- represent benthic communities typically smothered by sand de- gion, particularly in field sites where multiple specimens and posited by waning storm surges. Fossils are also preserved on the surfaces can be excavated and studied, such as the coastal ex- base of the beds of the sheet-sand facies, where fluidized sand posure in eastern , the White Sea region of north- smothered benthic communities in deeper water, well below western Russia, the Nilpena site in the Flinders Ranges of South wave base. Australia, and the Aar Farm site in southern Namibia. Excavation of 28 fossiliferous beds 4–25 m2 in area within these two facies demonstrates marked heterogeneity in both Heterogeneity of the Ediacaran Seafloor: An Example from abundance and diversity between beds (Fig. 2). Within each fa- the Ediacaran of South Australia cies, successions of beds of nearly identical sedimentology sug- One of the defining characteristics of the Ediacara Biota fossils is gest the possibility there was “community-scale” differentiation that they are typically preserved in situ. As a result, extensive of taxa in the Ediacara , where taxa were responding to bedding preserve individual communities as accurately as small-scale changes in environmental conditions, resulting in is possible in the fossil record. The Flinders Ranges region of a patchy distribution of taxa. These bedding plane data provide South Australia contains one of the best-exposed and most com- an unusually good opportunity to examine abundance diversity plete successions of to early rocks in the relationships, as time-averaging can be assumed to be as minimal world and includes the type section for the Ediacaran Period. as possible. Rarefied generic diversity curves indicate consider- Ediacara fossils occur within the Ediacara Member of the Rawnsley able variation between beds, but overall, the wave-base facies has Quartzite, preserved within a succession of shallow marine and a greater diversity overall than the sheet-sands facies (Fig. S1). deltaic facies and representing common components of the White Individual beds of the Ediacara Member exhibit a wide range of Sea Assemblage. evenness values (Fig. S2). Although beds with low evenness and Well-known fossils of the Ediacara Member, including Dick- high dominance are not rare, there are beds with evenness values insonia (Fig. 1A), Kimberella (Fig. 1D), Parvancorina (Fig. 1C), on par with those of the . Furthermore, although Spriggina (Fig. 1G), and other taxa, occur abundantly on the base these data are not similarly collected, the results are consistent of thin-bedded rippled quartz representing with the suggestion of Powell and Kowalewski (50) that evenness EVOLUTION EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES

Fig. 2. The relative abundance of different fossils on the excavated beds from South Australia. The total number of fossils found on the bed is given in parentheses after the bed name. All the beds shown, with the exception of the beds represented by the four right columns, represent deposition between fair-weather and storm wave base [the wave-base sand facies of Gehling and Droser (19)]. The four beds on the right are within the sheet-flow sand facies. The body fossil Funisia is preserved on beds MM2, Matt, and STC-X in abundances that range in the thousands, and thus, these fossils actually dominate beds. However, their dense packing and typically poor preservation do not allow for accurate counts on these beds.

Droser and Gehling PNAS | April 21, 2015 | vol. 112 | no. 16 | 4867 Downloaded by guest on October 2, 2021 increases through time (Fig. S2). In most Ediacaran cases, the continued excavation at various sites, these types of studies have same taxa are present on most of the beds, but it is the varying the promising potential to elucidate the biology of these - abundances of each that characterize these assemblages. For isms, if not the phylogeny, providing another step toward un- example, Dickinsonia and the holdfast both occur derstanding the link with Cambrian and younger animals. on nearly all of the beds, but in some cases, Dickinsonia domi- nates beds and in others, Aspidella dominates, indicating the Skeletonization and a Link to the Cambrian presence of abundant organisms. The apparent lack of taxonomic continuity between the Pre- Both the bed heterogeneity data and evenness values show cambrian and Cambrian fossil records has led to controversial that even though these represent nearly the oldest animal com- and conflicting interpretations about the Ediacara biota and munities (following on the heels of those of the Avalon As- their place in the evolution of metazoan life on this planet. This semblage), there is a sophistication of community assembly on has been further complicated by the absence of similar modes of par with that of the Phanerozoic. This is striking, considering the construction between these and the rarity of Precambrian lack of evidence for , infaunalization, and widespread skeletonized fossils. A relatively new Ediacara fossil, Corona- skeletonization. Although there is little evidence of interactions acula, described by Clites and colleagues (27), is preserved between taxa, there are abundant indications that several of the in the Ediacara Member (Rawnsley Quartzite) of South Australia taxa were interacting with the mat. and represents the oldest multielement (Fig. 3). Coro- nacollina consists of a triradial truncated cone associated with Population Structure and Reproduction ruler-straight spicules, up to 37 cm in length, diverging radially Preservation of extensive bedding planes also permits analysis of from the cone. The spicules most commonly disarticulated after large numbers of a single in situ. Funisia dorothea (Fig. 1B) and only rarely are found attached to the truncated cone. occurs in huge abundance on a number of bedding planes. It is The morphologic consistency between articulated and dis- up to 30 cm long and 12 mm in diameter and is divided longi- articulated spicules suggests they were made of a rigid substance, tudinally into serial units 6–8 mm in length throughout the length such as opaline silica or . In life, the spicules likely of the tube (Fig. 1B). Units within the tube decrease in width provided structural support in a manner similar to the Cambrian progressively toward the apex, suggestive of growth via terminal , . Although generally preserved flattened, Choia addition. Individuals can occur within dense assemblages, specimens from the Cambrian of Morocco 2 sometimes greater than 1,000/m . Funisia tubes are directly exhibit raised central regions, perhaps representing soft tissue connected to attachment structures that range from 1 to 8 mm. replaced by pyrite. The presence of Ediacaran -grade Importantly, attachment structures of a similar size and de- organisms has been suggested by both biomarkers (52) and other velopmental are spatially clustered, even within individual body fossils. A recent review questions the Poriferan origin of many bedding surfaces. of these taxa, suggesting that some are, for example, holdfasts or The phylogenetic affinity of F. dorothea is problematic. The microbial in origin (53). However, the sharply preserved spiculate lack of evidence for polypoid openings or pores in the body wall structures and the of preservation in some of these taxa such limits our understanding of its taxonomic affinities. However, as Paleophragmodictya cannot be easily reconciled with organic fibers, although it is difficult to place these fossils within Metazoa, the , or microbial structures or a holdfast origin. Constructed morphology and ecology are suggestive of cnidarian or poriferan grade animals. The branching patterns and rarity of branching of Funisia is consistent with metazoan asexual budding. The con- sistency of tube widths on individual bedding surfaces, the densely packed nature of the attachment structures, and the clustering pattern of developmental stages of attachment struc- tures on individual bedding planes suggests the juveniles settled as aggregates in a of limited cohorts. These solitary organisms thus exhibit growth by the addition of serial units to tubes and by the division of tubes, and dispersed propagation via the production of spats. Among living organisms, spat production is almost ubiquitously the result of sexual re- production but is known to occur rarely in association with asex- ual reproduction. Hence, despite its morphologic simplicity, the F. dorothea provides evidence of a variety of growth modes and a complex arrangement for the propagation of new individuals. Aggregation is not uncommon among some elements of the Ediacara biota, being present in the frondose holdfast Aspidella. These typically occur in dense assemblages, but in contrast to F. dorothea, their right skewed size distribution is consistent with continuous recruitment, rather than being periodic (18). Re- cently, Darroch and colleagues (51) analyzed the population structures of three rangeomorph taxa and one nonrangeomorph from Mistaken Point, using the Bayesian Information Criterion likelihood-based model selection. They found that although the populations of these taxa had wide distributions, each population was best described as a single distribution. The authors suggest that, assuming these organisms reproduced sexually, their findings Fig. 3. C. acula represents the oldest evidence of skeletonization. (A)A most strongly support a continuous or -round reproduction reconstruction of C. acula, after Clites and colleagues (27). This reconstruc- strategy for these taxa, as this would allow for unimodal populations tion is based on known specimens that have only up to four spicules, but it is with large overall size ranges. likely it had more. (B) The holotype SAM P43257 of C. acula. The central Only a few studies of large numbers of individual taxa pre- depression is the mold of the thimble-like main body of the specimen. Note served on a single bedding plane have been done. However, with the rigid spicules that radiate from the main body.

4868 | www.pnas.org/cgi/doi/10.1073/pnas.1403669112 Droser and Gehling Downloaded by guest on October 2, 2021 from a framework of rigid and brittle elements, Coronacollina reveals bedding surfaces with or without body fossil impressions. a constructional mode only recently recognized among members of Uniquely, Helminthoidichnites is preserved on bed soles as SPECIAL FEATURE the Ediacara biota. It provides a link in constructional mode across groove and levee and shows alternation of relief, but only when the Cambrian boundary and sheds light on the development of the sandstone layer is less than 15 mm thick and not covering an structural support in early . Although in many respects entire bed. This association is interpreted as a product of mat morphologically simple, Coronacollina is nonetheless one of the most mining by an animal too small to be characterized from casts and complicated of the Ediacara taxa because it was composed of at least molds and limited by the state within partly buried mat two different materials: the soft-bodied truncated cone, which was substrates. On the basis of fine-grained sandy layers, scalloped solid enough to withstand compaction, and biomineralized spicules. levees enable the direction of burrowing to be determined (Fig. Mobility and the Presence of Bilaterians 1I, Upper Left). On bed tops, Helminthoidichnites displays evi- dence of avoidance behavior exhibited by parallel spirals and The majority of organisms comprising the Ediacara Biota are interpreted to represent stationary or attached organisms. changing depth where crossings occurred. These traces are However, it now appears that at least four different Ediacaran common in the younger Ediacaran formations from relatively organisms were capable of movement. The association of certain shallower-water environments such as the Ediacara Member of body fossil taxa with motility and feeding traces provides the the Rawnsley Quartzite in South Australia (19), the Blueflower earliest evidence that the Ediacara Biota included bilaterian-grade Formation of the Mackenzie Mountains of northwest animals. External molds of Kimberella (Fig. 1D)havebeendocu- (60), and the Shibantan Member of the Dengjing Formation in mented in close association with casts of arrays of fanned sets of south China (61, 62). It is unlikely these complicated but de- bifid scratch traces (Kimberichnus teruzzii;Fig.1F)fromthe finitive trace fossils could have been made by anything other than Ediacara Member of the Rawnsley Quartzite, South Australia, a bilaterian. and the Verkhovka Formation, Zimnie Gory Formation, and in The serial arcuate looping forms, Paleopascichnus and Yelo- the basal part of the Erga Formation of the White Sea region of vichnus, and chains hemispheres, referred to as Neonereites, are northwestern Russia. From their orientation and proximity, these now considered encrusting body fossils, reinterpreted as xen- body and trace fossils are interpreted as evidence of mat grazing ophyophores by Seilacher and colleagues (63), but disputed by activities (31, 54, 55). The suggestions of molluscan affinities for Antcliffe and colleagues (64). The oldest described trace fossils Kimberella (23, 24, 53) should not overlook some important dif- seem to be those of actinian-grade polyps that left simple straight ferences from extant gastropod grazing behaviors (31, 56). Two or curved locomotive trails in ash-coated, deep-water substrates genera of the so-called dickinsoniomorphs, Dickinsonia (Fig. 1A) in the assemblage in southeastern and , are preserved as external molds at the end of serial sets Newfoundland (65). of roughly oriented faint casts of what are interpreted as “resting” or “feeding” traces, where these organisms remained stationary for Concluding Remarks periods of time, decomposing the substrate, before Taken as a whole, the Ediacara Biota represents an enigmatic moving to the next site, until the sediment-smothering events that “ ” assemblage of fossils that are not easily related to modern taxa.

preserved them and their footprints (57). Suggestions that these EVOLUTION However, examination of aspects of the ecology, such as trace are evidence of fungal “fairy-rings” (58), or random products of wave or current transport (59), are easily countered by the repeated ob- fossils, taphonomy, and morphology, reveal that these fossils servation that the “footprints” were made in a definite order, as show characteristics of modern taxa. It is clear that bilaterians, determined by identification of the body axis and anterior enlarge- cnidarians, and poriferans are represented among the Ediacara ment of body divisions in these organisms. The implication that the Biota. Although we may never be able to reconcile the phylogeny mat on the substrate decomposed sufficiently to enable a cast sug- of all, or even most, of the Ediacara taxa, it is likely that with gests that such a process could have been a source of nutrition for these approaches, we will be able to continue to better relate dickinsoniids. Alone among the Ediacara biota, dickinsoniids feature these taxa with both modern and extinct animals.

preserved external body molds with apparent contraction marks and EARTH, ATMOSPHERIC, variable patterns of body divisions that might be explained by mus- ACKNOWLEDGMENTS. We are indebted to Jane and Ross Fargher for access to AND PLANETARY SCIENCES their property. Fieldwork was facilitated by D. Rice, M. Dzaugis, M. E. Dzaugis, cular peristaltic contraction. There is no equivalent evidence of dif- P. Dzaugis, D. A. Droser, R. Droser, V. Droser, C. Droser, N. Anderson, E. Gooch, ferential contraction of body elements among the array of taxa of C. Casey, M. Laflamme, J. Doggett, J. Paterson, C. Armstrong, J. Perry, D. Reid, , such as Pteridinium (Fig. 1H)andPhyllozoon (9). J. McEntee, I. Smith, M. Fuller, P. Trusler, members of the South Australian The most abundant trace fossils in shallow marine environ- Museum Waterhouse Club, and the Ediacaran Foundation. S. Finnegan, L. Tarhan, and C. Hall aided with this manuscript. The research was supported by ments associated with rich assemblages of the Ediacara Biota are National Science Foundation Grant EAR-0074021, NASA Grant NNG04GJ42G very common groove and levee trails of Helminthoidichnites (Fig. NASA Exobiology Program (to M.L.D.), and Australian Research Council 1I) that are found in both part and counterpart on numerous Discovery Grant DP0453393 (to J.G.G.).

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