The Neoproterozoic Cyanobacteria Have Not Changed Many Large Gaps We Have in Our Morphologically in Over 3 Billion Years

Current Biology Magazine

cyanobacteria today? Certainly, it Across these geological timescales, would be diffi cult to assume that it is important to be frank about the The Neoproterozoic cyanobacteria have not changed many large gaps we have in our morphologically in over 3 billion years. understanding of the evolutionary Nicholas J. Butterfi eld Although there are many lines of succession of life. Truly, it is remarkable evidence suggesting that life arose how much we have already been able The Neoproterozoic era was arguably during the Archean, it is important to to piece together through varying fi elds the most revolutionary in Earth history. highlight the uncertainty surrounding spanning biology, paleontology, and Extending from 1000 to 541 million Archean microfossils as evidence of geosciences. The diffi culty in studying years ago, it stands at the intersection early life. these ancient questions should not of the two great tracts of evolutionary Other lines of evidence have stemmed deter us from studying them, but rather time: on the one side, some three from molecular fossils — the presence inspire us to continually fi nd alternative billion years of pervasively microbial and identifi cation of complex organic ways of studying them in order to test ‘Precambrian’ life, and on the other biological molecules (i.e., biomarkers) in prior assumptions about the robustness the modern ‘Phanerozoic’ biosphere sediments, used to date the existence of of previous hypotheses. If anything, with its extraordinary diversity of large certain organisms. Biomarkers make the advances in our understanding of early multicellular organisms. The disturbance assumption that molecules could only life will be interesting in light of newly doesn’t stop here, however: over this have been produced by certain lineages. developed techniques and the growing same stretch of time the planet itself was Ideally, biomarkers would provide the abundance of sequence data to begin in the throes of change. Tectonically, chemical fi ngerprints necessary to testing assumptions we have had with it saw major super-continental identify the microbes living in ancient us for decades. reconfi gurations, climatically its deepest sediments. This assumption has been ever glacial freeze, and geochemically challenged with the gradual acceptance some of the most anomalous of the fact that lateral gene transfer is FURTHER READING perturbations on record. What lies behind nearly ubiquitous across all bacteria. this dramatic convergence of biological Canfi eld, D.E. (2014). Oxygen: A Four Billion Year Correspondingly, some of the most History (Princeton: Princeton University Press). and geological phenomena, and how important cyanobacterial biomarkers Canfi eld, D.E., and Teske, A. (1996). Late exactly did it give rise to the curiously (i.e., 2-methylhopanes) have been Proterozoic rise in atmospheric oxygen complex world that we now inhabit? concentration inferred from phylogenetic and shown to be present in other bacterial sulphur-isotope studies. Nature 382, 127–132. Like all historical reconstructions, phyla. This example highlights how our Dalton, R. (2002). Microfossils: Squaring up over any useful study of the Neoproterozoic ancient life. Nature 417, 782–784. incomplete understanding of extant life Des Marais, D.J. (2000). When did photosynthesis requires a chronological framework can easily alter our interpretations of emerge on earth? Science 289, 1703–1705. to keep things in order (Figure 1). ancient life. Johnston, D.T., Wolfe-Simon, F., Pearson, A., and To a fi rst approximation, the fi rst Knoll, A.H. (2009). Anoxygenic photosynthesis It is impossible to get away from modulated Proterozoic oxygen and sustained half of the era — the Tonian — uncertainty when examining the Earth’s middle age. Proc. Natl. Acad. Sci. USA appears to represent Proterozoic 106, 16925–16929. evidence for early life. This is just the Johnson, J.E., Webb, S.M., Thomas, K., Ono, business as usual, a continuation nature of the subject matter. With this in S., Kirschvink, J.L., and Fischer, W.W. (2013). of the Mesoproterozoic status quo. mind, it becomes even more important Manganese-oxidizing photosynthesis before the Evidence from microfossils (Figure rise of cyanobacteria. Proc. Natl. Acad. Sci. USA to understand the challenges and 110, 11238–11243. 2A,F,G), chemical fossils (primarily nuances in interpreting the evidence Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B., lipid biomarker molecules) and used in generating further hypotheses and Worm, B. (2011). How many species are sedimentology (stromatolites and other there on Earth and in the ocean? PLoS Biol. 9, on early life. e1001127. microbial mat fabrics) point to on-going Novacek, M.J. (2001). The Biodiversity Crisis: Losing monopolization of marine productivity What Counts (New York: The New Press). Conclusion Planavsky, N.J., Reinhard, C.T., Wang, X., Thomson, by cyanobacteria, while geochemical Phototrophy has sustained life on D., McGoldrick, P., Rainbird, R.H., Johnson, T., proxies document extensively stratifi ed Earth, possibly since the dawn of life. Fischer, W.W., and Lyons, T.W. (2014). Low Mid- oceans with free oxygen limited largely Proterozoic atmospheric oxygen levels and the Archean ecosystems were most likely delayed rise of animals. Science 346, 635–638. to its sun-lit surface layers. Tonian-age sustained by anoxygenic phototrophic Rashby, S.E., Sessions, A.L., Summons, R.E., eukaryotes are recognizable in the form organisms which may have grown in and Newman, D.K. (2007). Biosynthesis of sterane biomarkers and protistan- of 2-methylbacteriohopanepolyols by an stromatolites much like modern day anoxygenic phototroph. Proc. Natl. Acad. Sci. grade microfossils (Figure 2B–D,H,I), microbial mats. With the innovation of USA 104, 15099–15104. but show little inclination to diversify Shih, P.M., and Matzke, N.J. (2013). Primary the oxygen-evolving complex, oxygenic endosymbiosis events date to the later or expand their decidedly marginalized photosynthesis provided the biological Proterozoic with cross-calibrated phylogenetic Mesoproterozoic footprint. There is catalyst to accumulate oxygen in dating of duplicated ATPase proteins. Proc. Natl. no sign of multicellular animals or Acad. Sci. USA 110, 12355–12360. the atmosphere. These metabolic land plants at this stage, and rates of inventions provided profound shifts in evolutionary turnover are fundamentally how once purely abiotic geochemical 1Joint BioEnergy Institute, 5885 Hollis lower than in the subsequent fossil 2 cycles would integrate the evolution St, Emeryville, CA 94608, USA. Physical record. The supercontinent Rodinia Biosciences Division, Lawrence Berkeley of life to ultimately transform into the National Laboratory, One Cyclotron Rd, begins to break up in the middle of the global biogeochemical cycles we Berkeley, CA 94720, USA. Tonian, around 850 million years ago, observe today. E-mail: [email protected] but with little obvious impact to the

Bilateria Rodinia

Cnidaria

Porifera Breakup

δ13C Gaskiers Marinoan +5

0 Mesoproterozoic Palaeozoic -5 Sturtian giaciation ?

Tonian Cryogenian Ediacaran Cambrian 1000 million years ago 750 635 541 Current Biology

Figure 1. The Neoproterozoic. Diagram of the Neoproterozoic Era illustrating the large scale correlation between evolutionary innovation, climate perturbation, and trends in the 13C of marine carbonates (a refl ection of the global carbon cycle). Patterns in the distribution of protistan-grade fossils are depicted below the 13C curve and include pre-Cryogenian ornamented microfossils (orange; typically asymmetrical, moderately large and stratigraphically long-lived), ‘vase-shaped’ microfossils (purple), scale microfossils (green), Ediacaran-age ornamented and ‘embryo’ microfossils (red; typically symmetrical and large, with ‘embryos’ sometimes occurring within the lumen of ornamented forms), Ediacaran macrofossils (grey), and ornamented Cambrian microfossils (dark orange; typically symmetrical and small). Bars above the 13C curve represent molecular clock estimates for the fi rst appearance of major metazoan groups (from Erwin et al. 2011), with white stars marking the fi rst ‘suggestive’ occurrence of corresponding fossils, and red stars indicating fi rst ‘convincing’ occurrence of such fossils. 13C data taken primarily from Halverson et al. (2010) and Lenton et al. (2014), with early Tonian data from Xiao S. et al. (2014) Biostratigraphic and chemostratigraphic constraints on the age of early Neoproterozoic carbonate successions in North China. Precambrian Res. 246, 208–225. Note that there are substantial dif- ferences of opinion over the stratigraphic correlation of much of the data depicted here, particularly with respect to the age-range of Ediacaran microfossils and the relationship between the Gaskiers glaciation and carbon isotope excursions. The boundary between the Tonian and the Cryogenian has yet to be formally defi ned. The dashed line at ~530 million years ago marks the onset of rapid evolutionary change, and regime shift into recognizably Phanerozoic style ecological and evolutionary dynamics, the ‘Cambrian Explosion’, as well as return to the relatively equable 13C expression of the early Tonian. The end of the Neoproterozoic Era (and Proterozoic Eon) is coincident with the beginning of the Palaeozoic Era (and Phanerozoic Eon). system beyond increased variability in ice-sheets repeatedly fl owed into tropical measure, the Ediacaran was eventful, marine carbon isotope values (Figure 1). (palaeo-)latitudes, with the accompanying experiencing one further short-lived All this begins to change at around ice-albedo feedbacks potentially driving glaciation (the Gaskiers), the assembly of 750 million years ago. For the fi rst sea-ice cover and runaway ‘Snowball- a new supercontinent (Gondwanaland), time, biomarker data show eukaryotes Earth’ conditions. There were two main conspicuous geomagnetic anomalies, contributing quantitatively to export phases of Cryogenian glaciation (the and a world-class meteorite impact. production — the primary productivity Sturtian and Marinoan; Figure 1), both All this, however, was eclipsed by that sinks out of the surface ocean — of which ended abruptly with ice- contemporaneous biogeochemistry. while protistan diversity expands to transported tillite deposits immediately Over a few tens of millions of years the include conspicuously armoured testate overlain by distinctive limestone and carbon isotope values of sedimentary ameobae and biomineralizing ‘scale dolomite sediments — so-called rocks appear to abandon uniformitarian microfossils’ (Figure 2E,J). Although ‘cap-carbonates’ — indicative of theory, recording unparalleled highs and anoxia remains the default condition particularly warm-water conditions. Such lows, a bizarre decoupling of the organic- of the deeper ocean, geochemical juxtaposition points to a large-scale carbon and carbonate-carbon reservoirs signatures point to a signifi cant increase instability in global climate — a hysteresis and the largest ever continuous fall in in oxygen availability towards the separating two alternative stable states. background values, the ‘Shuram/Wonoka surface. Increasingly high carbon- negative isotope excursion’ (Figure 1). isotope values through the course of the The Ediacaran At the same time, baseline sulfur isotope Tonian, accompanied by increasingly By international agreement, the base values became anomalously heavy, pronounced falls, document major shifts of the ‘cap-carbonate’ overlying the deep marine environments became in the marine carbon cycle (Figure 1). Marinoan glaciation marks the beginning progressively oxygenated, and there was And at around 720 million years ago, the of the Ediacaran Period — the fi nal ~90 unprecedented deposition of sedimentary planet tips into the extreme icehouse million-year interval of the Neoproterozoic phosphates across much of the planet. conditions of the Cryogenian (Figure 1). and its stratigraphic connection to the Not surprisingly, the Ediacaran was Over the next 80 million years continental Phanerozoic (Figure 1). By any sort of also marked by dramatic shifts in the

AB C D E

F H I J

Figure 2. Representative Tonian and Cryogenian microfossils. (A) Colonial spheroids, possibly cyanobacterial from the ~850 million year-old Wynniatt Formation, NW Canada. (B) Leiosphaeridia sp., a relatively large spheroidal microfossil probably (but not demonstrably) the remains of a unicellular photosynthetic eukaryote, from the ~820 million year-old Svanbergfjellet Formation, Spitsbergen. (C) Germinosphaera fi brilla, an ornamented eukaryote of unknown affi nity, from the Svanbergfjellet Forma- tion. (D) Trachyhystrichosphaera aimika, an ornamented eukaryote with a late Mesoproterozoic to late Tonian age-range (~1100 to 720 million years ago), from the Svanbergfjellet Formation. (E) Characodictyon skolopium, a phosphatic ‘scale microfossil’ from the ~720 million year-old Fifteen Mile Group, NW Canada. (F) Eohyella rectoclada, a pseudo-fi lamentous cyanobacterium, from the ~800 million year-old Limestone-Dolomite Series, East Greenland. Image: Andy Knoll. (G) Filamentous mat, most likely cyanobacterial, from un-named Tonian strata, NW Canada. (H) Cerebrosphaera buicki, a distinctively wrinkled (probable) eukaryote with a mid- to late-Tonian age-range (~820 to 720 million years ago), from the Svanbergfjellet Formation. (I) Cymatiosphaeroides kullingii, a multi-enveloped eukaryote with a mid- to late-Tonian age-range, from the Fifteen Mile Group. (J) A vase-shaped microfossil (VSM), probably a testate amoeba, from the early Cryogenian Visingso Group, Sweden. Image: Monica Marti Mus. (Scale bar: A = 100 µm; B = 160 µm; C = 300 µm; D = 350 µm; E = 1200 µm; F = 170 µm; G = 230 µm; H = 145 µm; I = 300 µm; J = 950 µm.) fossil record. Although cyanobacteria it is not at all clear what living groups most clearly in the form of simple but continued to play a major role as primary of organisms they are related to, nor convincing bilaterian burrows beginning producers, biomarker data point to even how they made a living. Although around 555 million years ago (Figure 3F). increasingly greater contributions by a few can be reasonably interpreted as Sediment-disrupting trails in ~565 million eukaryotic algae. Few of the distinctively multicellular animals or seaweeds, most year old sediments from Newfoundland eukaryotic microfossils known from pre- have an underlying fractal or tubular type were most likely formed by cnidarian-like glacial strata survive into the Ediacaran, of construction with no obvious modern animals (Figure 3G), while a single ~600 but these are more than made up for by analogues — and at least some lived million year old phosphatized microfossil a pronounced radiation of much more in conspicuously deep water settings, from South China (Figure 3A) is exotically ornamented forms (Figure 3B), ruling out a phototrophic mode of life. currently the best body-fossil evidence controversial ‘embryo microfossils’, One intriguing possibility is that these for pre-Cambrian sponges — a data which may or may not be metazoan fractal and tubular forms represent point supported by apparent sponge- (Figure 3C), and, most strikingly, the fi rst an independent, and ultimately failed, specifi c biomarkers identifi ed in terminal appearance of genuinely macroscopic evolutionary experiment in eukaryotic Cryogenian and younger strata. A variety organisms. First seen in the aftermath multicellularity. Another is that they of shelly fossils of probable sponge of the Gaskiers glaciation, these constitute the extinct stem-group forms and cnidarian affi liation appear in the centimeter- to metre-sized ‘Ediacaran of higher order modern taxa, e.g., later Ediacaran (Figure 3D,E) and, like macrofossils’ comprise three loosely stem-group Fungi, Metazoa, Porifera or bilaterian trace fossils, show a modest defi ned assemblages of soft-bodied Eumetazoa. degree of diversifi cation through to the forms that persisted through to the end Bona fi de crown group animals do end of the period. Ironically, there is no of the period (Figure 3H–J). Even so, appear in the Ediacaran, however, fundamental change in palaeontological

A BIG H

D EF J

Figure 3. Representative Ediacaran fossils. (A) Eocyathispongia qiania, a phosphatized sponge-grade fossil from the ~600 million year-old Doushantuo Formation, South China. Image: Zongjun Yin. With permission from Yin et al. (2015). (B) Mengeosphaera reticulata, an ornamented eukaryote of unknown affi nity from the Doushantuo Forma- tion. Image: Shuhai Xiao. (C) Megasphaera/Parapandorina, a eukaryotic ‘embryo’ fossil that has been variously interpreted as a crown-group metazoan, a ‘non-metazoan holozoan’, and a photosynthetic protist; in some instances, these fossil occur with the lumen of ornamented microfossils; from the Doushantuo Formation. Image: Shuhai Xiao. (D) A tentaculate compression fossil, possibly of cnidarian-grade, from the early Ediacaran Lantian biota, South China. Image reprinted by permission of Macmillan Publishers Ltd: Nature,Yuan et al. 2011, copyright 2011. (E) Cloudina cari- nata, a biomineralizing cnidarian-grade fossil from the ~542 million year-old, Ibor Group, central Spain. Image: Ivan Cortijo. (F) A simple horizontal burrow, most likely produced by a bilaterian animal, from the ~555 million year-old Ediacaran Hills, South Australia. Image: Soren Jensen. (G) A simple horizontal trace fossil with a meniscate fabric, most likely produced by cnidarian-grade animal, from the ~565 million year-old, Mistaken Point Formation, SE Newfoundland. Image: Alex Liu. (H) Charnia masoni, a fractally constructed Ediacaran macrofossil and constituent of the deep-water ‘Avalonian biota’ of Charnwood Forest, UK (~565 million years old). Image: Phil Wilby. (I) Pteridinium simplex, a three-dimensionally preserved Edi- acaran macrofossil with a quilted construction from the ~550 million year-old Nudas Formation, Namibia. Image: Dima Grazhdankin. (J) Dickinsonia costata, an Ediacaran macrofossil with apparent bilateral symmetry and localized evidence of intermittent movement, from the ~ 555 million year-old Verkhovka Formation, NW Russia. Image: Dima Grazhdankin. (Scale bars: A = 200 µm; B = 115 µm; C = 290 µm; D = 4.5mm; E = 1.5 mm; F = 8.5 mm; G = 4.5 mm; H = 1.5 cm; I = 1.9 cm; J = 1 cm.) expression marking the stratigraphically events from residually biased data, and biogeochemical dynamics. The ratifi ed end of the Neoproterozoic, and superimposing a storyline that real question, then, is what tipped despite the iconic status of the sensibly accounts for the patterns. the pre-Cryogenian system out of ‘Precambrian–Cambrian’ boundary. In Certainly there are important feedback its longstanding equilibrium — and qualitative terms, the Neoproterozoic era effects between the various biological at what level early animal evolution only properly draws to a close with the and geological compartments, and is interwoven with other aspects of ‘explosive’ radiation of animals — and there is little question that the Tonian Neoproterozoic history. associated return to pre-Cryogenian and Cambrian represent ‘alternative Animals are fundamentally aerobic levels of biogeochemical stability stable states’ of the global biosphere, organisms and there is a long tradition of (Figure 1) — some 10 million years into separated by ~200 million years of explaining their origins in terms of oxygen the early Cambrian (see accompanying transitional Cryogenian–Ediacaran availability. Indeed, current molecular Primer by Briggs in this issue). instability. Moreover, it is clear that the clock estimates for the evolutionary fi rst Cambrian explosion itself does not appearance of animals (see reviews by An evolutionary synthesis require any special explanation. It is Lee and Palci, and Telford et al. in this As with all ancient histories, the simply an adaptive radiation of animals, issue) coincide intriguingly with the onset challenge of the Neoproterozoic lies and their increasingly pronounced of mid-Neoproterozoic perturbations in in reconstructing the true course of feedbacks on ecological, evolutionary marine redox signatures and the marine

carbon cycle in general (Figure 1). matter transferring a major fraction of biogeochemical cycles under increasingly Likewise, the appearance of Ediacaran biological oxygen demand from the regulated biological control. In terms of macrofossils and the Cambrian radiations water column into the benthos. At the proximal causation, the only necessary have regularly been tied to subsequent same time, such differential fi ltering addition to Neoproterozoic history may ‘oxygenation events’. Such ‘permissive fundamentally recasts plankton ecology, have been the gene regulatory networks environment’ scenarios offer an intuitively with selective advantage shifting from necessary to build this revolutionary new satisfying account of how increases in default cyanobacterial picoplankton clade of organisms. atmospheric oxygen might account for to the larger-celled eukaryotic algae key evolutionary innovations through excluded by the small sieve-size FURTHER READING the Neoproterozoic. Even so, there are of sponges. Taken together, the some awkward explanatory gaps. Why, evolutionary appearance of sponge-type Butterfi eld, N.J. (2009). Oxygen, animals and oceanic for example, did simple sponge-grade fi lter feeding would have revolutionized ventilation: an alternative view. Geobiology 7, 1–7. Butterfi eld, N.J. (2011). Animals and the invention of animals with vanishingly low oxygen contemporaneous marine structure, the Phanerozoic Earth system. Trends Ecol. Evol. requirements take so long to evolve? tipping primary productivity from its 26, 81–87. Even the most generous interpretation longstanding cyanobacterial condition Canfi eld, D.E., Poulton, S.W., and Narbonne, G.M. (2007). Late-Neoproterozoic deep-ocean of the fossil record and molecular clocks to an alternative stable state in which oxygenation and the rise of animal life. Science puts the fi rst appearance of sponges eukaryotes thrive, oxygen minimum 315, 92–95. Erwin, D.H., and Tweedt, S. (2011). Ecological drivers back no further than the late Tonian, zones are suppressed, and marine-shelf of the Ediacaran-Cambrian diversifi cation of a billion years after the last common environments become progressively Metazoa. Evol. Ecol. 26, 417–433. ancestor of (aerobic) eukaryotes. ventilated. Erwin, D.H., Lafl amme, M., Tweedt, S.M., Sperling, E.A., Pisani, D., and Peterson, K.J. (2011). The Moreover, there is a good argument In this light, there is indeed a causal Cambrian conundrum: early divergence and later for viewing limited oxygen availability correlation between the perturbations of ecological success in the early history of animals. Science 334, 1091–1097. not so much as an impediment to the Cryogenian–Cambrian Earth system Feulner, G., Hallmann, C., and Kienert, H. (2015). sponge-grade multicellularity, but as and early animal evolution, though not Snowball cooling after algal rise. Nat. Geosci. 8, a condition likely to encourage it: by in the simple oxygen-driven fashion in 659–662. Halverson, G.P., Wade, B.P., Hurtgen, M.T., actively driving water currents through which it is most often presented. By and Barovich, K.M. (2010). Neoproterozoic their aquiferous systems, sponges recognizing the pervasive effects of chemostratigraphy. Precambrian Res. 182, gain access to fundamentally greater animals on Earth-surface processes, 337–350. Knoll, A.H., Walter, M.R., Narbonne, G.M., and amounts of oxygen than their unicellular many of the interconnecting threads of Christie-Blick, N. (2006). The Ediacaran Period: a counterparts, without sacrifi cing overall Neoproterozoic history can be reconciled new addition to the geologic time scale. Lethaia 39, 13–30. surface area or substantially increasing in terms of step-wise biological Lenton, T.M., Boyle R.A., Poulton, S.W., Shields-Zhou, metabolic demand. Conversely, if innovation and its compounding G.A., and Butterfi eld, N.J. (2014). Co-evolution early animal evolution is meant to be a feedback on both the environment and of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265. consequence of Cryogenian-Cambrian other organisms. The marked expansion Mills, D.B., Ward, L.M., Jones, C., Sweeten, B., Forth, oxygenation events, it would seem to of eukaryotes beginning in the late M., Treusch, A.H., and Canfi eld, D.E. (2014). Oxygen requirements of the earliest animals. Proc. require an extraordinarily rapid assembly Tonian, for example, is most simply Natl. Acad. Sci. USA 111, 4168–4172. of their underlying (and uniquely explained as a ‘top down’ consequence Planavsky, N.J., Reinhard, C.T., Wang, X., Thomson, complex) developmental programs once of earliest animal evolution, while D., McGoldrick, P., Rainbird, R.H., Johnson, T., Fischer, W.W., and Lyons, T.W. (2014). Low Mid- the putative threshold levels had been its cascading effects on the marine Proterozoic atmospheric oxygen levels and the attained. biological pump, or even atmospheric delayed rise of animals. Science 346, 635–638. The other factor regularly left out of albedo via the enhanced production of Sperling, E.A., Wolock, C.J., Morgan, A.S., Gill, B.C., Kunzmann, M., Halverson, G.P., Macdonald, F.A., the equation is the powerful top-down cloud condensation nuclei, may have Knoll, A.H., and Johnston, D.T. (2015). Statistical ‘engineering’ effects that animals impart, triggered the succeeding Cryogenian analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, both on the physical environment and glaciations. The accompanying 451–454. other organisms. Most modern marine expansion of oxygenated habitat Tziperman, E., Halevy, I., Johnston, D.T., Knoll, A.H., sediments, for example, owe their undoubtedly facilitated the appearance and Schrag, D.P. (2011). Biologically induced initiation of Neoproterozoic snowball-Earth events. chemistry and fabric to the burrowing of Ediacaran macro-organisms in Proc. Natl. Acad. Sci. USA 108, 15091–15096. activities of large bilaterian animals, deeper water, but there is no direct Xiao, S., Muscente, A.D., Chen, L., Zhou, C., which, in turn, owe their large size evidence for increasing shallow-water Schiffbauer, J.D., Wood, A.D., Polys, N.F., and Yuan, X. (2014). The Weng’an biota and the and diversifi ed habits to escalatory (or indeed atmospheric) oxygenation Ediacaran radiation of multicellular eukaryotes. predator–prey interactions. Sponges, through the Neoproterozoic. Certainly, Nat. Sci. Rev. 1, 498–520. Yin, Z., Zhu, M., Davidson, E.H., Bottjer, D.J., Zhao, ctenophores and cnidarians exhibit threshold levels of oxygen were a F., and Tafforeau, P. (2015). Sponge grade body fundamentally less disruptive behaviours prerequisite for the evolution of more fossil with cellular resolution dating 60 Myr before than bilaterians, but even these simple active and metabolically demanding the Cambrian. Proc. Natl. Acad. Sci. USA 112, E1453–E1460. animals are major agents of (aquatic) marine animals, but the appearance Yuan, X., Chen, Z, Xiao, S., Zhou, C., Hua, H. (2011). bioturbation. In the case of sponges, of cnidarian- and bilaterian-grade An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes. both active and passive pumping animals was also accompanied by Nature 470, 390–393. moves enormous volumes of seawater fundamentally more sophisticated means through their fi nely channelized for acquiring such limiting resources, for Department of Earth Sciences, University of tissue, with the selective extraction of constructively re-engineering previously Cambridge, Cambridge CB2 3EQ, UK. picoplankton and dissolved organic hostile environments, and for bringing E-mail: [email protected]