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Darroch Et Al 2018 TREE TREE 2407 No. of Pages 11 Opinion Ediacaran Extinction and Cambrian Explosion 1, 2 3 4 Simon A.F. Darroch, * Emily F. Smith, Marc Laflamme, and Douglas H. Erwin The Ediacaran–Cambrian (E–C) transition marks the most important geobio- Highlights logical revolution of the past billion years, including the Earth’s first crisis of We provide evidence for a two-phased bioticturnovereventduringtheEdiacaran- macroscopic eukaryotic life, and its most spectacular evolutionary diversifica- –Cambrian transition (about 550–539 tion. Here, we describe competing models for late Ediacaran extinction, Ma),whichbothcomprisestheEarth’sfirst major biotic crisis of macroscopic eukar- summarize evidence for these models, and outline key questions which will yotic life (the disappearance of the enig- drive research on this interval. We argue that the paleontological data suggest matic ‘Ediacara biota’) and immediately – – two pulses of extinction one at the White Sea Nama transition, which ushers precedes the Cambrian explosion. in a recognizably metazoan fauna (the ‘Wormworld’), and a second pulse at the Wesummarizetwocompetingmodelsfor E–C boundary itself. We argue that this latest Ediacaran fauna has more in the turnover pulses – an abiotically driven ‘ common with the Cambrian than the earlier Ediacaran, and thus may represent model(catastrophe)analogoustothe Big 5’ Phanerozoic mass extinction events, the earliest phase of the Cambrian Explosion. and a biotically driven model (biotic repla- cement) suggesting that the evolution of Evolutionary and Geobiological Revolution in the Ediacaran bilaterian metazoans and ecosystem The late Neoproterozoic Ediacara biota (about 570–539? Ma) are an enigmatic group of soft- engineering were responsible. bodied organisms that represent the first radiation of large, structurally complex multicellular We summarize the evidence in support eukaryotes. Although many of these organisms may represent animals (Metazoa), few share of both models and identify several key any synapomorphies with extant metazoan clades and thus may represent extinct groups with research questions which will help to distinguish between them, and thus no modern representatives [1] (Figure 1). Consequently, the position of the Ediacara biota in the shed light on the origins of the modern, context of the late Neoproterozoic–Cambrian rise of animals remains poorly understood. After animal-dominated biosphere. nearly 30 million years (my) as the dominant components of benthic marine ecosystems, the Ediacara biota disappeared in the first major biotic transition of complex life, succeeded by a We argue that the first turnover pulse (about 550 Ma) marks the greatest spectacular biotic radiation – the ‘Cambrian Explosion’ – which marks the appearance of a change in organismal and ecological majority of extant animal clades and the establishment of metazoan-dominated ecosystems complexity, leading to a more recog- [2,3]. Understanding the cause(s) behind the disappearance of the Ediacara biota and its nizably metazoan global fauna that has relationship to the subsequent Cambrian radiation is thus key to understanding the origins of much more in common with the Cam- brian than the earlier Ediacaran. This the modern biosphere, and is an important research goal in geology, paleontology, and latest Ediacaran interval (the ‘Nama’) evolutionary biology. However, the mechanisms behind this transition are poorly understood, may therefore represent the earliest with recent research providing support for different models. One model posits an abiotic driver phase of the Cambrian Explosion. similar to the causes of the Phanerozoic ‘Big 5’ mass extinctions (hereafter termed the 1 ‘ ’ – – catastrophe model ), while a separate but not necessarily mutually exclusive scenario Vanderbilt University, Nashville, TN 37235-1805, USA invokes a biotic driver linked to the radiation of metazoans with new behaviors and feeding 2 Johns Hopkins University, Baltimore, modes (the ‘biotic replacement’ model). An alternative model suggesting that the apparent MD 21218-2683, USA 3 extinction is an artifact of a closing preservational window has been rejected, on the basis that University of Toronto Mississauga, Mississauga, ON L5L 1C6, Canada Ediacaran-style matgrounds (and thus the conditions necessary for fossilization) persist into the 4 Smithsonian Institution, PO Box Cambrian [4]. The catastrophe model would place the Cambrian Explosion as a postextinction 37012, MRC 121, Washington, DC fi fi diversi cation, similar in form if greatly different in result, to the early Cenozoic diversi cations of 20013-7012, USA birds and placental mammals. By contrast, a biotic replacement model potentially creates a more gradual transition from the latest Ediacaran faunas into the earliest Cambrian. Here, we *Correspondence: synthesize recent work on this interval and identify a series of fundamental research goals. [email protected] Answering these questions will shed light on the sequence of events leading to the origin of (Simon A.F. Darroch). Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy https://doi.org/10.1016/j.tree.2018.06.003 1 © 2018 Elsevier Ltd. All rights reserved. TREE 2407 No. of Pages 11 (A) (B) (C) (D) (E) (F) (H) (G) (I) (J) (K) (M) (L) Figure 1. Enigmatic Fossils from the Ediacaran. (A–D) Soft-bodied Ediacara biota belonging to the ‘White Sea’ assemblage, and which disappear prior to the onset of the late Ediacaran ‘Nama’ interval about 550 Ma (A, Andiva; B, Dickinsonia; C, Yorgia; D, Tribrachidium). (E–H) Soft-bodied erniettomorph and rangeomorph Ediacara biota belonging to the relatively species-poor ‘Nama’ assemblage (E, Swartpuntia; F, Rangea; G, Ernietta; H, Pteridinium). (I–M) Characteristic metazoan (See figure legend on the bottom of the next page.) 2 Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy TREE 2407 No. of Pages 11 modern-looking ecosystems, as well as add valuable new information on the processes that have driven both mass extinctions and evolutionary radiations over the last about 550 my. Ediacaran–Cambrian Bioevents The Ediacaran [635–539? million years ago (Mya)] marks the transition from Proterozoic to Phanerozoic, and is the most recently named geological period. The base of the Ediacaran is defined by a Global Boundary Stratotype Section and Point (GSSP) in South Australia marking the end of the Marinoan Snowball Earth glaciation [5], while its top (and base of the Cambrian) is intended to coincide with the first appearance of the trace fossil Treptichnus pedum in southeast Newfoundland [6,7]. Fossils of soft-bodied Ediacara biota first appear in the Avalon Peninsula (Newfoundland) in sequences that overly diamictite recording the Gaskiers glaciation. Recent dates from the Avalon and Bonavista peninsulas give a maximum age of 570.94 Æ 0.38 Ma for the first appearance of Ediacaran fossils [8]. New ashes that have been dated at the onset and at the 13 nadir of the basal Cambrian d C excursion in South China constrain this secondary chronostrati- graphic marker of the Ediacaran–Cambrian (E–C) boundary to about 539 Ma, consistent with re- dated ashes from southern Namibia [9]. Within this interval, three temporally and faunally distinc- tive assemblages have been recognized: the ‘Avalon’, ‘White Sea’, and ‘Nama’ [10,11] (Figure 2). The White Sea assemblage (about 558–550 Ma) marks the apex of Ediacaran diversity, with many iconic groups (sometimes clades, see [12]), such as the Dickinsonimorpha, Bilateromorpha, and Triradialomorpha, well represented. By contrast, the youngest Ediacaran assemblage – the Nama (550–539? Ma) – contains a relatively species-poor community overwhelmingly dominated by the Rangeomorpha and Erniettomorpha, with many other Ediacaran groups apparently already extinct [13,14]. The Nama assemblage also records a proliferation of organic-walled tubular organisms, a diversification in bilaterian trace fossils [15], and the appearance of the calcifying invertebrates Cloudina, Namacalathus, and Namapoikia, marking a fundamental shift to commu- nities with a much higher proportion of metazoans [16–18]. This proliferation of vermiform metazoans has led to the latest Ediacaran Nama assemblage being referred to as ‘Wormworld’ and may indicate an escalation in metazoan ecosystem engineering and the evolution of the Eltonian pyramid (i.e., the appearance of primary and secondary metazoan consumers) [19]. With a few rare (and contested) exceptions, the Ediacara biota disappear entirely at the Cambrian boundary, along with the majority of the ‘Wormworld’ fauna [20–23]. We argue that the biostratigraphic evidence points to two episodes of biotic turnover and extinction: one at about 550 Ma at the transition between the White Sea and Nama assemb- lages, and a second at the E–C boundary itself. This second event was closely followed by the Cambrian Explosion, marked by the appearance of a diverse array of metazoan groups, and the most dramatic interval of metazoan morphologic innovation in the history of life [24]. Ediacaran–Cambrian Record of Environmental Change One of the great challenges of the E–C transition is understanding the possible causal connections between the dramatic biotic shifts and coeval environmental changes. One feature of Phanerozoic mass extinctions is that they are frequently accompanied by negative carbon isotope excursions, which record perturbations to global marine oceans. Rather than exploring the list of possible environmental triggers for the Cambrian radiation, we focus our discussion
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