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TREE 2407 No. of Pages 11

Opinion

Ediacaran and Explosion

1, 2 3 4

Simon A.F. Darroch, * Emily F. Smith, Marc Laflamme, and Douglas H. Erwin

The –Cambrian (E–C) transition marks the most important geobio- Highlights

logical revolution of the past billion , including the ’s first crisis of We provide evidence for a two-phased

bioticturnovereventduringtheEdiacaran-

macroscopic eukaryotic , 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 .

in a recognizably metazoan (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’ mass extinction events,

the earliest phase of the Cambrian Explosion.

and a biotically driven model (biotic repla-

cement) suggesting that the of

Evolutionary and Geobiological Revolution in the Ediacaran bilaterian metazoans and ecosystem

The late 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

. Although many of these organisms may represent (Metazoa), few share

of both models and identify several key

any synapomorphies with extant metazoan 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

-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 , , and

latest Ediacaran interval (the ‘Nama’)

evolutionary . 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 (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,

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 diversi cations of 20013-7012, USA

and placental . By contrast, a biotic replacement model potentially creates a

more gradual transition from the latest Ediacaran into the earliest Cambrian. Here, we

*Correspondence:

synthesize recent work on this interval and identify a 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 , 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 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, ; B, ; C, ; D, ). (E–H) Soft-bodied erniettomorph and

Ediacara biota belonging to the relatively -poor ‘Nama’ assemblage (E, ; F, ; G, ; H, ). (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 to

Phanerozoic, and is the most recently named . The base of the Ediacaran is

defined by a Global Boundary Stratotype Section and Point (GSSP) in marking the

end of the Marinoan glaciation [5], while its top (and base of the Cambrian) is

intended to coincide with the first appearance of the trace pedum in southeast

Newfoundland [6,7]. Fossils of soft-bodied Ediacara biota first appear in the

() in sequences that overly diamictite recording the . 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 constrain this secondary chronostrati-

graphic marker of the Ediacaran–Cambrian (E–C) boundary to about 539 Ma, consistent with re-

dated ashes from southern [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 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

Cloudina, , and , 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 [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

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

here on the two large, possibly global perturbations to the at the close of the

Proterozoic: the Shuram and the Basal Cambrian Carbon Isotope Excursion (the ‘BACE’).

‘Wormworld’ body fossils and trace fossils that existed alongside Ediacara biota in the Nama assemblage, representing the onset of , diversification of

feeding behaviors, and intensification of animal ecosystem engineering (I, Gaojiashania; J, Namacalathus; L, unnamed ; K, Shaanxilithes; M, large,

treptichnid-like traces from the late Ediacaran of Namibia). Filled scale bars 1 cm, open 5 mm.

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Carbon isotope Metazoans and Global diversity ‘Ediacara biota’ (δ13C) record ‘ecosystem engineering’

Calcifying Organic-walled 0 20 40 60 80 100 120 metazoans metazoans 40 20 0 529 529 (’Wormworld’fauna)

533 533 Fortunian Cambrian ? Cambrian 538 ? 538 ? ? ‘BACE’

543 ons 543 Ɵ

‘Wormworld’ omorpha nc Ʃ Nama Nama Ɵ Ex

548 Rangeomorpha 548 Ernie Arboreomorpha ? ? 553 553 Time (mya) Cloudina Wutubus ‘Shuram’ Conotubus Namacalathus White Sea White Sea White

558 Gaojiashania 558 ‘Complex’ burrowing Sekwitubulus Ediacaran Ediacaran Pentaradialomorpha Tetraradialomorpha Plausible metazoans Shaanxilithes

Ediacara biota Macroscopic 563 563 Avalon Avalon

568 Bilateromorpha 568 Triradialomorpha Dickinsonimorpha 571 0 20 40 60 80 100 120 4 0 4 880 4 0 4 4 0 4 2 0 2 4 0 4 440 4 0 4 -12 -6 0 +6 40 20 0

# Genera # Genera δ13C (‰VPDB) # Bilaterian ichnogenera

Figure 2. Ediacaran–Cambrian Timescale. This illustrates the stratigraphic distribution and gamma diversity of enigmatic Ediacaran groups (Ediacara biota), the

more recognizably metazoan ‘Wormworld’ fauna (both ‘calcifying’ and ‘organic-walled’ metazoans), diversity of bilaterian ichnogenera, and the onset of putative

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‘ecosystem engineering’ effects, alongside the record of environmental perturbation (as compilation d C curve). Diversity of Ediacara biota and bilaterian ichnogenera

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replotted from [11] and [15], respectively. d C data compiled by [26] and [58]. BACE, Basal Cambrian Carbon Isotope Excursion; mya, million years ago; VPDB, Vienna

Pee Dee Belemnite standard.

The Shuram event is a large negative carbon isotope excursion that reaches values as low as

À12m, much lower than the modern mantle carbon value of À5m [25]. This excursion is

commonly thought to end at about 551 Ma [26], however, there are poor radiometric age

constraints for its onset, duration, and return to baseline values; better age constraints are

critical for demonstrating its global synchroneity [27]. Diagenesis has been proposed as a

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possible explanation for the extreme negative d C values (e.g., [28]). More recently, however,

Ca and Mg isotopic data have been used to argue for a primary of the Shuram [29]. What

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remains to be determined is whether or not the Shuram d C values recorded isotopic values of

global dissolved inorganic carbon (DIC) at the time of deposition or, as has been suggested for

other large Proterozoic excursions, a local phenomenon [30].

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The BACE, a negative d C excursion that accompanies the biotic shift that occurs across the

E–C boundary [31], has better radiometric constraints than the Shuram, but is similarly lacking a

mechanistic explanation. As with the Shuram, it is not clear whether this signal is primary or

diagenetic, local or global in nature.

Competing Models for End-Ediacaran Transition

Several alternative scenarios have been posited for the shift between the Ediacara and earliest

Cambrian biotas. An abiotic driver of extinction is invoked by the ‘catastrophe’ model,

potentially represented by the Shuram and/or the BACE. If globally synchronous, these

excursions represent major perturbations to the global carbon cycle, and could reflect a variety

of possible kill mechanisms. The ‘biotic replacement’ model, by contrast, suggests that biotic

modification of substrate and other environments by emerging metazoans may have been

responsible. Ecosystem engineering encompasses physical, ecological, and chemical modifi-

cation of their environment by organisms, which may create, modify, or destroy habitats for

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TREE 2407 No. of Pages 11

other organisms [33,34]. Unlike much of the Ediacara biota, which were dominantly sessile and

used only a limited variety of feeding modes [21], many extant metazoan groups have important

ecosystem engineering and trophic impacts. Examples include the ability to vertically mix the

sediment column (thus aerating the subsurface and creating new habitat), actively ‘pumping’

water to aid in filter feeding (removing suspended organic matter and ventilating the water

column), and predatory feeding modes, which can precipitate predator–prey arms races, or

alternatively eliminate prey species that are unable to adapt [19]. Although there is no direct

evidence for the early bilaterians recorded in the Nama ‘Wormworld’ outcompeting Ediacara

biota in the Ediacaran [35], this model suggests that the activities of evolving metazoans were

deleterious to soft-bodied Ediacara biota and led to their disappearance prior to the Cambrian.

These differences in extinction drivers between competing models – ‘catastrophe’ and ‘biotic

replacement’ – can be illustrated using the predicted trajectories of both soft-bodied Ediacara

biota and the burgeoning Cambrian-style metazoan fauna (Figure 3). ‘Biotic replacement’

predicts that depauperate latest Ediacaran ecosystems reflect a fauna that was being

progressively stressed, marginalized, and replaced, while also showing increased evidence

for diversification and ecosystem engineering by new metazoan lineages. By contrast,

‘catastrophe’ would predict that Ediacaran ecosystems should remain relatively high diversity

and ‘unstressed’ until the E–C boundary, at which point environmental disturbance triggers

extinction in both Ediacara biota and metazoans alike. These scenarios are end members of a

continuum, with additional permutations possible: the simple ‘catastrophe’ model does not

account for the two apparent episodes of extinction, and sequential environmental events

(pulsed catastrophe) may have driven biotic turnover at the start and end of the Nama interval

(represented by the Shuram and BACE events, respectively).

The differences in extinction models can also (potentially) be distinguished on the basis of rate

and timing of biotic turnover. Of the ‘big 5’ Phanerozoic events known to have been caused by

‘catastrophe’-type events – for example, the – (P–T) and –Paleo-

gene (K–Pg) – the rate of ecosystems collapse is fast on geological timescales (virtually

3 4

instantaneous in the K–Pg, and about 10 –10 years in the case of the P–T, see [36]).

Consequently, a ‘catastrophe’-type event in the Late Ediacaran might be expected to result

in geologically rapid turnover. ‘Biotic replacement’, by contrast, relies on the appearance of

new behaviors and traits in multiple metazoan clades, and therefore might be expected to result

5 6

in more protracted biotic turnover on evolutionary timescales (10 –10 years). However, this

latter point is more speculative, because unlike ‘catastrophe’, large-scale ‘biotic replacement’

has no direct analog in the Phanerozoic. Although some authors [14] have suggested that the

ongoing diversity crisis (the ‘6th mass extinction’) might represent a similar process, the extent

to which current extinction rates are comparable with mass extinctions in the geological past is

uncertain [37], and thus we argue that ‘fast’ and ‘slow’ are useful predictions for each model.

In the following sections, we outline several key questions that will help discriminate between

these models, resolve the cause(s) of the E–C transition, and shed new light on the drivers of

(and links between) mass extinctions and subsequent diversification.

Key Questions and Research Priorities for the Ediacaran–Cambrian

What, and When, Was the Shuram?

Can the large environmental perturbations represented by the Shuram be stratigraphically and

radiometrically linked to the biotic shift, and possible , that happens across the

White Sea–Nama transition? This interval is thought to coincide with the Shuram excursion [38],

but radiometric constraints on the Shuram are poor, with some estimates placing the start of

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1.) ‘Catastrophe’ Metazoan ‘ecosystem engineers’ (abundance/evenness/diversity)

Ediacara biota Community metric

2.) ‘Pulsed catastrophe’ Metazoan ‘ecosystem engineers’

Ediacara biota

3.) ‘BioƟc replacement’ Metazoan ‘ecosystem engineers’

Ediacara biota

White Sea Nama Cambrian Ediacaran

550Age (Ma) 530

Figure 3. Modeled Trajectories of Different Biological Groups (Ediacara Biota and Cambrian-Style

Metazoan ‘Ecosystem Engineers’) and Predicted Fossil Community Responses (Community Metric), under

Three Proposed Extinction Scenarios. Figure modified from [3].

the excursion at about 560–550 Ma [26,39], while others suggesting that Shuram-like excur-

sions may have begun as early as about 609 Ma [40], predating the Gaskiers glaciation. In

sections where the Shuram and Ediacaran fossils are both present, the excursion is typically

finished before White Sea assemblage fossils appear [41]. In addition, some studies suggest

that the Shuram may have been a protracted event lasting up to about 50 my [40]. With its

extreme nadir and unusually long duration, the Shuram requires either an Ediacaran carbon

cycle fundamentally different from the modern one (e.g., [25]), a global diagenetic event [42], or

the product of authigenic carbonate formation [43,44]. Adequately testing this facet of the

‘catastrophe’ hypothesis requires (i) establishing radiometric ages on the onset and termination

of the Shuram; (ii) demonstrating that the Shuram is synchronous globally; and (iii) linking these

environmental changes with the fossil record (see Outstanding Questions).

What, and When, Was the BACE?

Until it has been demonstrated that it is a synchronous global chemostratigraphic marker, it is

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not clear whether the d C chemostratigraphic profiles that have been documented across

several E–C boundary sections record coeval changes in DIC (e.g., [30]). Although the BACE

has better radiometric age constraints than the Shuram excursion [9,20,45], it has not been

precisely dated radiometrically in more than one region. If it is established that BACE records a

global signature of DIC, follow-up questions about its driving mechanism and causal relation-

ship to biotic turnover can be addressed, including: (i) What is the extent and pace of biotic

turnover? Does abrupt biotic turnover coincide with an environmental perturbation

[20,22,46,47], or is the biotic transition gradual and uncorrelated to environmental changes?

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[31]; (ii) What is the mechanism driving the BACE? Only with absolute ages can the carbon

fluxes, reservoir sizes, and oxidant demands needed to drive the BACE and other large E–C

excursions be rigorously constrained (e.g., [48]).

Can We Disentangle Correlation versus Causation in the Late Ediacaran Extinction Event?

Establishing proximal extinction drivers is a major challenge in deciphering the causes of biotic

turnover in the late Ediacaran. In terms of ‘catastrophe’, establishing a temporal correlation

between isotope excursions and biotic impact is crucial, however, this says little about

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causation. Taking the P–T mass extinction (251 Ma) as an example, a negative d C change

at the end-Permian has been convincingly linked to volcanism associated with the Siberian

Traps; this in turn drove global warming, ocean acidification, elevated carbonate saturation

states, and primary productivity collapse, all of which would have devastated the biosphere and

comprised proximal extinction drivers [36,49]. However, establishing similar causal connec-

tions in the late Ediacaran is far more challenging, not least from the difficulty of finding sections

where it is possible to link geochemical proxies with the paleontological record. Considerable

debate persists over the mechanism causing the Shuram excursion, and similar problems are

associated with the source of the BACE [22]. This uncertainty in the ultimate source of

perturbation to the late Ediacaran carbon cycle renders any discussion of proximal extinction

drivers associated with them speculative.

Inferring extinction drivers associated with ‘biotic replacement’ is no easier. Although the

diversification of metazoan trace and body fossils in the Nama indicates an escalation in

metazoan ecosystem engineering, how this may have affected the soft-bodied Ediacara biota

has not been established. Suggestions that expansion of grazing and burrowing in metazoans

disrupted microbial matgrounds that served as food for some Ediacaran organisms have been

largely rejected, since similar substrates persisted into the Cambrian [4]. Given the discovery of

drill holes in biomineralizing Cloudina [50] it is tempting to suggest the evolution of macroscopic

metazoan predation as a plausible extinction driver, however, no fossil evidence has been

found for metazoans preying directly on soft-bodied Ediacarans (in fact, slabs preserving both

Ediacara biota and bilaterian trace fossils in the Nama are rare, suggesting a degree of niche

partitioning [35]). Although there is some limited evidence for large populations of metazoan

passive predators living in the same communities as Ediacara biota (and thus possibly

representing a significant ecological pressure upon Ediacaran larvae in the water column –

see [35]), these sorts of biotic interactions are hard to demonstrate convincingly.

In sum, although demonstrating a close temporal correlation between isotope excursions and

global faunal turnover may be enough to support the ‘catastrophe’ model, support for ‘biotic

replacement’ will hinge on demonstrating a plausible extinction driver stemming from early

animal activity. Interrogating the ‘biotic replacement’ model thus necessitates a deeper under-

standing of Ediacaran paleoecology, in particular establishing how the Ediacara biota inter-

acted with the emerging metazoan fauna. Interestingly, examining the survivors of the first

extinction pulse may be a key to understanding the proximal extinction drivers associated with

either the ‘catastrophe’ or ‘biotic replacement’ models. Although many Ediacaran groups

apparently perished during the White Sea–Nama transition, the Rangeomorpha and Ernietto-

morpha survived; representatives of these groups have been found in Nama-aged assemb-

lages on three paleocontinents, suggesting that they are some of the few Ediacaran organisms

to have persisted into the metazoan-dominated ‘Wormworld’. These two clades may have

been ecological generalists (in terms of habitat preferences and/or modes of nutrient acquisi-

tion) [14], or may have possessed characteristics that made them resistant to the stresses

associated with the extinction pulse (e.g., tolerance to low ). Either way, establishing

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how and why these groups survived will offer valuable clues as to why many others did not. New

techniques involving computational fluid dynamics [51,52] provide a powerful new way of

examining Ediacaran (including determination of feeding mode and mobility), and

so offer one potential way forward to testing these hypotheses.

What Role Did End-Ediacaran Extinction Play in the Cambrian Explosion?

Several of the Phanerozoic ‘Big 5’ mass extinctions were followed by the origin of new clades,

expansions of morphologic disparity, and rapid diversification of new taxa. For example,

bivalves show transient increases in origination rate after the three most recent mass extinction

events [53]. Given that the Cambrian Explosion remains one of the most rapid and dramatic

biotic radiations in Earth history, there has been speculation that this event may have been

triggered by environmental perturbation across the E–C boundary (e.g., [46]). However,

demonstrating this has remained elusive; small shelly faunas show a relatively steady pattern

of diversification across the E–C transition [32], and there is little evidence for a postmass

extinction ecological vacuum or ‘disaster fauna’ in the earliest Cambrian. In addition, the overall

notion of ecological opportunity as a driver of biotic radiations is being re-evaluated, with the

recognition that most are associated with macroevolutionary ‘lags’ between the first appear-

ance of new organismal traits and their eventual ecological dominance. This suggests that

morphological novelty often arises long before the environmental or ecological conditions that

might guarantee their success [54]. The discovery that many complex bilaterian behaviors that

were initially thought to be restricted to the Cambrian actually arose in the late Ediacaran about

548 Ma (albeit in a primitive/preliminary form; see [55]) supports the notion that forerunners to

the Cambrian were present millions of years before the Cambrian boundary.

That Cambrian-type metazoan organisms are present and apparently diversifying in the latest

Ediacaran poses an alternative question: does the Nama ‘Wormworld’ interval represent the

earliest phase of the Cambrian Explosion? Although opinion is still divided on whether many of

the White Sea fauna represent metazoans (Box 1), the appearance of biomineralization,

macroscopic predation, and complex, Treptichnus-like burrowing behaviors are arguably

metazoan traits that have far more in common with the Cambrian evolutionary fauna than

the Ediacaran White Sea fauna preserved in South Australia and Russia. If all the ecological and

evolutionary changes that take place over the Ediacaran and Cambrian are considered

Box 1. Which of the Ediacara Biota Represent Metazoans?

Despite >80 years of study the biological affinities of the Ediacara biota remain enigmatic, principally because few share

any synapomorphies with Phanerozoic animal groups. Some, however, do preserve characters that align them with

metazoan phyla that subsequently diversify in the Cambrian. Among these, (IV) is the best candidate for a

bilaterian metazoan, possessing a number of mollusk-like characteristics: Kimberella was likely mobile, preserves

evidence for a muscular ‘foot’, and is commonly associated with scratch marks (Kimberichnus isp.), illustrating

possession of paired radula-like structures. Other Ediacaran groups, however, possess body plans entirely unknown

among extant metazoan phyla. For example, the Rangeomorpha (I) are a that possesses ‘fractal’ morphology

composed of self-similar frondlets, while the Erniettomorpha are constructed from unbranched cylindrical modules

arranged in leaflike sheets. Although the Dickinsonimorpha (V), Triradialomorpha (VI), and Bilateromorpha (VII) have all at

one time been placed somewhere on the metazoan tree (e.g., the Dickinsonimorpha with , see [59]), there has

been no scientific consensus on these placements (Figure I). As a result, there is currently no basis for assigning these

groups to the Metazoa. We therefore split soft-bodied Ediacaran fossils in Figure 2 into either ‘Ediacara biota’ (genera

with no incontrovertible metazoan synapomorphies) or ‘plausible metazoans’. The former group includes many iconic

Ediacaran fossils, such as Dickinsonia, Tribrachidium, and Rangea (Figure 1), while the latter includes Kimberella, as well

as possible such as , Rugoconites, and Paleophragmodictya. The distinctive tubular and calcifying

forms of the ‘Wormworld’ fauna during Nama time are likely metazoans (for example, [18]). Splitting the Ediacaran fossil

assemblage in this way oversimplifies much of the phylogenetic uncertainty surrounding some of these organisms,

however, it illustrates the rise of organisms in the late Ediacaran, which bear a stronger resemblance to the Cambrian

evolutionary fauna.

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Outstanding Questions

Paleophragmodictya Inaria Kimberella What, and when, was the Shuram?

II III IV

What, and when, was the BACE?

Can we disentangle correlation and

causation in Ediacaran extinction?

What role did end-Ediacaran extinction

Bilateria play in the Cambrian Explosion? Porifera Placozoa Lophotrochozoa Ecdysozoa Deuterostomia

Rangeomorpha? Avalofractus Examples of unknown

I groups V VI VII

Dickinsonia Tribrachidium

Figure I.

together, it could be argued that the biggest change in organismal and ecological complexity

arrives at the White Sea–Nama boundary, rather than at the E–C boundary itself. In this context,

establishing the timing and driver of the Shuram excursion takes on added importance, as in

this scenario it would coincide not only with the earliest major turnover in complex macroscopic

life, but also with the onset of the most dramatic in Earth History.

Concluding Remarks

Understanding the drivers and pacing of late Ediacaran extinction, as well as how it is

connected to the evolutionary radiation that followed, will reveal the origins of the modern

metazoan-dominated biosphere. On the one hand, support for the ‘catastrophe’ model would

illustrate a crucial role played by environmental fluctuations in driving early metazoan evolution.

On the other, support for ‘biotic replacement’ would instead represent the first evidence for a

biological driver of mass extinction, and suggest that evolutionary innovation, ecosystem

engineering, and biological interactions ultimately caused the first major biotic turnover of

complex life. However, we also note that these two models are not mutually exclusive; either or

both could be operating in the late Ediacaran and be responsible for either of the two turnover

events. Even more intriguingly, the two could be mechanistically linked – the effects of

on sediment and ocean chemistry are well known (e.g., [56]), and so a model

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TREE 2407 No. of Pages 11

whereby the evolution of new metazoan behaviors were responsible for perturbations to the

global carbon cycle (the Shuram and BACE) is one that deserves testing. In summary, the E–C

transition is undoubtedly a complex interval and determining between abiotic and biotic drivers

will be challenging. However, the questions we pose above are all readily answerable with new

data, and the recent discovery of continuous sections through the E–C boundary preserving

both a rich fossil assemblage and a detailed chemostratigraphic record [57] offers much

promise for understanding this critical interval in Earth History.

Acknowledgments

S.A.F.D. acknowledges generous funding from National Geographic (Grant No. 9968-16), and a Paleontological Society

Arthur Boucot Award. E.F.S. was supported by the Smithsonian Institution Peter Buck Fellowship Program and The

Palaeontological Association (Award ID PA-RG201703). M.L. acknowledges funding from NSERC Discovery Grant

(RGPIN 435402). D.H.E. was supported by NASA through National Astrobiology Institute (Grant No. NNA13AA90A)

to the MIT node. This manuscript was considerably improved after constructive reviews by Susannah Porter and two

anonymous reviewers.

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