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The Advent of Animals: the View from the Ediacaran SPECIAL FEATURE

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The Advent of Animals: the View from the Ediacaran SPECIAL FEATURE The advent of animals: The view from the Ediacaran SPECIAL FEATURE Mary L. Drosera,1 and James G. Gehlingb,c aDepartment of Earth Sciences, University of California, Riverside, CA 92521; bSouth Australia Museum, Adelaide, 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 evolution of early complex life on this relationships within the Ediacara Biota and, importantly, reveals the planet are largely interpreted from the fossils 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 organisms living in marine environments. classified with modern taxa, they nonetheless provide the record Although these exceptionally preserved fossil 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, ecology, and taphonomy 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 animal evo- y range of the Ediacara Biota, fossils of these multicellular organisms lution is offered by examination of the paleoecology, 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 ecosystems, 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 | South Australia | 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 Flinders Ranges of South Australia, the White Sea Fphologically diverse and generally soft-bodied organisms (1) Region of Russia, and Namibia (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 Precambrian (2). The record of these organisms predates assemblages: the Avalon, the White Sea, and the Nama, which the well-known Cambrian 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 genus and species level. The phologic [e.g., rangeomorphs and arboreomorphs (cf. 21)] types. apparent discontinuity between the Precambrian and the Cam- Particularly striking are the common fractal-like self-similar brian fossil record is largely based on the absence of skeletal hard branching rangeomorph 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 bacteria. Although Cambrian-type constructional morphologies among the Ediacara this feeding type is restricted to these bacteria in the modern era, – 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 extinction of early ani- 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 Cnidaria, predates the well-known Cambrian Explosion by nearly 40 and segmented forms with generally bilateral symmetry have been million years and provides critical information concerning early associated with annelids and arthropods (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 biology unusual style of preservation as casts and molds in medium-grained and/or ecology similar to animals today, and some were most sandstone, prompted suggestions of a wide range of alternative certainly bilaterians, cnidarians, and poriferans. phylogenetic affinities, ranging from an extinct kingdom of “Ven- dobionts” (10) to prokaryotic colonies (11), protists (12), lichens 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 fauna 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, clades (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 carbon 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 trace fossil 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 bear 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,
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