WHAT SPARKED THE EXPLOSION? An evolutionary burst 540 million ago filled the seas with an astonishing diversity of . The trigger for that revolution is finally coming into focus.


of dark, craggy pinnacles rises oceans held so little that modern modern anatomical features. The Cambrian 80 metres above the grassy plains would have quickly foundered and died there. explosion, as it is called, produced of . The peaks call to mind A gooey mat of microbes covered the sea floor, with legs and compound , worms with Asomething ancient — the burial mounds of and on that blanket lived a variety of enigmatic feathery gills and swift predators that could past civilizations or the tips of vast pyramids animals whose bodies resembled thin, quilted crush prey in -rimmed jaws. Biologists buried by the ages. pillows. Most were stationary, but a few mean- have argued for decades over what ignited this The stone formations are indeed monu- dered blindly over the slime, grazing on the evolutionary burst. Some think that a steep rise ments of a faded empire, but not from anything microbes. was simple, and there in oxygen levels sparked the change, whereas hewn by hands. They are pinnacle reefs, were no predators. But an evolutionary storm others say that it sprang from the development built by cyanobacteria on the shallow sea floor would soon upend this quiet world. of some key evolutionary innovation, such as 543 million years ago, during what is known Within several million years, this simple eco- vision. The precise cause has remained elusive, as the period. The ancient world would disappear, and give way to a world in part because so little is known about the occupied by these reefs was truly alien. The ruled by highly mobile animals that sported physical and chemical environment at that time.

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The Cambrian seas But over the past steps, approaching today’s sea-surface concen- them, he found that tiny worms survive in areas teemed with new types several years, discov- trations at the start of the Cambrian, around 541 of the sea floor where oxygen levels are very low of animal, such as the eries have begun to million years ago — just before more-modern — less than 0.5% of average global sea-surface predator yield some tantalizing animals suddenly appeared and diversified. This concentrations. Food webs in these oxygen- (centre). clues about the end of supported the idea of oxygen as a key trigger for poor environments are simple, and animals feed the Ediacaran. Evi- the evolutionary explosion. directly on microbes. In places where sea-floor dence gathered from the Namibian reefs and But last , a major study1 of ancient oxygen levels are a bit higher — about 0.5–3% other sites suggests that earlier theories were sea-floor sediments challenged that view. of concentrations at the sea surface — animals too simplistic — that the Erik Sperling, a palaeontologist at Stanford are more abundant but their food webs remain actually emerged out of a complex interplay University in California, compiled a database limited: the animals still feed on microbes rather between small environmental changes that trig- of 4,700 iron measurements taken from rocks than on each other. But around somewhere gered major evolutionary developments. around the world, spanning the Ediacaran and between 3% and 10%, predators emerge and Some scientists now think that a small, Cambrian periods. He and his colleagues did start to consume other animals4. perhaps temporary, increase in oxygen sud- not find a statistically significant increase in the The implications of this finding for denly crossed an ecological threshold, enabling proportion of oxic to anoxic water at the bound- are profound, Sperling says.The modest oxygen the emergence of predators. The rise of carn­ ary between the Ediacaran and the Cambrian. rise that he thinks may have occurred just before ivory would have set off an evolutionary arms “Any oxygenation event must have been far, the Cambrian would have been enough to trig- race that led to the burst of complex body types far smaller than what people normally consid- ger a big change. “If oxygen levels were 3% and and behaviours that fill the oceans today. “This ered,” concludes Sperling. Most people assume they rose past that 10% threshold, that would is the most significant event in evolution,” “that the oxygenation event essentially raised have had a huge influence on early animal evo- says Guy Narbonne, a palaeobiologist at Queen’s oxygen to essentially modern- levels. And lution,” he says. “There’s just so much in animal University in Kingston, . “The advent of that probably wasn’t the case”, he says. ecology, lifestyle and body size that seems to pervasive carnivory, made possible by oxygena- The latest results come at a time when sci- change so dramatically through those levels.” tion, is likely to have been a major trigger.” entists are already reconsidering what was The gradual emergence of predators, driven happening to ocean oxygen levels during this by a small rise in oxygen, would have meant ENERGY TO BURN crucial period. Donald Canfield, a geobiol- trouble for Ediacaran animals that lacked obvi- In the modern world, it’s easy to forget that ous defences. “You’re looking at soft-bodied, complex animals are relative newcomers to mostly immobile forms that probably lived Earth. After life first emerged more than 3 bil- “This is the most their by absorbing nutrients through their years ago, single-celled organisms domi- significant event in skin,” says Narbonne. nated the planet for most of its history. Thriving Studies of the ancient Namibian reefs suggest in environments that lacked oxygen, they relied Earth evolution.” that animals were indeed starting to fall prey to on compounds such as dioxide, sulfur- predators by the end of the Ediacaran. When containing molecules or iron minerals that act ogist at the University of Southern Denmark palaeobiologist Rachel Wood from the Uni- as oxidizing agents to break down food. Much in Odense, doubts that oxygen was a limiting versity of Edinburgh, UK, examined the rock of Earth’s microbial biosphere still survives on factor for early animals. In a study published last formations, she found spots where a primitive these anaerobic pathways. month2, he and his colleagues suggest that oxy- animal called Cloudina had taken over parts of Animals, however, depend on oxygen — a gen levels were already high enough to support the microbial . Rather than spreading out much richer way to make a living. The process simple animals, such as , hundreds of over the ocean floor, these cone-shaped crea- of metabolizing food in the presence of oxygen millions of years before they actually appeared. tures lived in crowded colonies, which hid their releases much more energy than most anaero- Cambrian animals would have needed more vulnerable body parts from predators — an eco- bic pathways. Animals rely on this potent, con- oxygen than early sponges, concedes Canfield. logical dynamic that occurs in modern reefs5. trolled combustion to drive such energy-hungry “But you don’t need an increase in oxygen Cloudina were among the earliest animals innovations as muscles, nervous systems and across the Ediacaran–Cambrian boundary,” he known to have grown hard, mineralized exo- the tools of defence and carnivory — mineral- says; oxygen could already have been abundant skeletons. But they were not alone. Two other ized shells, and teeth. enough “for a long, long time before”. types of animal in those reefs also had min- Given the importance of oxygen for animals, “The role of oxygen in the origins of animals eralized parts, which suggests that multiple, researchers suspected that a sudden increase in has been heavily debated,” says Timothy Lyons, unrelated groups evolved skeletal shells around the amount of the gas in the oceans, to near- a geobiologist at the University of California, the same time. “Skeletons are quite costly to modern levels, could have spurred the Cam- Riverside. “In fact, it’s never been more debated produce,” says Wood. “It’s very difficult to come brian explosion. To test that idea, they have than it is now.” Lyons sees a role for oxygen in up with a reason other than defence for why an studied ancient ocean sediments laid down evolutionary changes, but his own work3 with animal should bother to create a skeleton for during the Ediacaran and Cambrian periods, molybdenum and other trace metals sug- itself.” Wood thinks that the skeletons provided which together ran from about 635 million to gests that the increases in oxygen just before protection against newly evolved predators. 485 million years ago. the Cambrian were mostly temporary peaks Some Cloudina from that period even In Namibia, and other spots around that lasted a few million years and gradually have holes in their sides, which scientists inter- the world, researchers have collected rocks stepped up (see ‘When life sped up’). pret as the marks of attackers that bored into the that were once ancient sea beds, and analysed creatures’ shells6. the amounts of iron, molybdenum and other MODERN MIRRORS Palaeontologists have found other hints that metals in them. The metals’ solubility depends Sperling has looked for insight into Ediacaran animals had begun to eat each other by the late strongly on the amount of oxygen present, so oceans by studying oxygen-depleted regions Ediacaran. In Namibia, Australia and New- the quantity and type of those metals in ancient in modern seas worldwide. He suggests that foundland in Canada, some sea-floor sediments sedimentary rocks reflect how much oxygen biologists have conventionally taken the wrong have preserved an unusual type of tunnel made was in the water, when the sediments formed. approach to thinking about how oxygen shaped by an unknown, wormlike creature7. Called These proxies seemed to indicate that oxy- animal evolution. By pooling previously pub- burrows, these warrens branch gen concentrations in the oceans rose in several lished data with some of his own and analysing again and again, as if a predator just below the

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When life sped up also possible that animals went in the opposite Big animals emerged during the Ediacaran period, but these creatures were slow or immobile. A rise in oceanic direction. Sperling says that the need to avoid NATURE oxygen concentrations at the end of the period might have helped to trigger the Cambrian evolutionary explosion. predators (and pursue prey) may have driven animals into the water column above the sea 80 635 Myr: A glacial bed, where enhanced oxygen levels enabled might have A gradual, NIK SPENCER/ 580 Myr: Large them to expend energy through swimming. 800 million years ended with a possibly uneven, Ediacaran animals 60 ago (Myr): Oxygen temporary spike in rise towards The emerging evidence about oxygen appeared. levels rose from oxygen. Other spikes modern levels. thresholds and ecology could also shed light less than 0.1% to could have happened 542 Myr: Extinction of on another major evolutionary question: when 40 perhaps 1–2%. at di erent times. Ediacaran animals. did animals originate? The first undisputed Start of Cambrian explosion. fossils of animals appear only 580 million 20 years ago, but genetic evidence indicates that oxygen concentrations oxygen basic animal groups originated as far back as

Percentage of modern ocean Percentage ? 0 700 million or 800 million years ago. Accord- Ediacaran Cambrian ing to Lyons, the solution may be that oxygen levels rose to perhaps 2% or 3% of modern lev- 800 700 600 500 400 els around 800 million years ago. These con- centrations could have sustained small, simple Ediacaran Cambrian animals, just as they do today in the ocean’s organisms organisms oxygen-poor zones. But animals with large • Had a , bodies could not have evolved until oxygen which is a sti , levels climbed higher, in the Ediacaran. internal rod Understanding how oxygen influenced the appearance of complex animals will require • Could grow to more Anomalocaris scientists to tease subtler clues out of the rocks. than 1 metre • Predator with eyes and circular jaws “We’ve been challenging people working on fossils to tie their fossils more closely to our • May have been a lter-feeding animal oxygen proxies,” says Lyons. It will mean deci- The Cambrian explosion produced many of phering what oxygen levels were in different The Ediacaran animals were the animal types common today, such as ancient environments, and connecting those relatively simple and lacked arthropods (Marrella and the Anomalocaris) • Small evidence of legs, eyes and many and (Pikaia), a group that now with feathery gills values with the kinds of traits exhibited by the other anatomical innovations includes . animal fossils found in the same locations. Late last year, Woods visited with had systematically probed for animals that grazed on the microbial mat. Early that goal in mind. She collected fossils of Clou- prey animals on top. The Treptichnus burrows trails from about 555 million years ago meander dina and another skeletonized animal, Suvo- resemble those of modern priapulid, or ‘penis’, and criss-cross haphazardly, indicating a poorly rovella, from the waning days of the Ediacaran. worms — voracious predators that hunt in a developed that was unable to The sites gave her the chance to gather fossils remarkably similar way on modern sea floors8. sense or react to other grazers nearby — let from many different depths in the ancient The rise of at this time put large, alone predators. But at the end of the Ediacaran ocean, from the more oxygen-rich surface sedentary Ediacaran animals at a big disadvan- and into the early Cambrian, the trails become waters to deeper zones. Wood plans to look tage. “Sitting around doing nothing becomes a more sophisticated: creatures carved tighter for patterns in where animals grew tougher liability,” says Narbonne. turns and ploughed closely spaced, parallel lines skeletons, whether they were under attack by through the sediments. In some cases, a curvy predators and whether any of this had a clear THE WORLD IN 3D feeding trail abruptly transitions into a straight link with oxygen levels. “Only then can you The moment of transition from the Ediacaran line, which Narbonne interprets as potential evi- pick out the story.” ■ to the Cambrian world is recorded in a series dence of the grazer evading a predator9. of stone outcrops rounded by ancient glaciers This change in grazing style may have Douglas Fox is a journalist in northern on the south edge of . Below that contributed to the fragmentation of the micro- California. boundary are impressions left by quilted Edi- bial mat, which began early in the Cambrian. acaran animals, the last such fossils recorded on And the transformation of the sea floor, says 1. Sperling, E. A. et al. Nature 523, 451–454 (2015). Earth. And just 1.2 metres above them, the grey Narbonne, “may have been the most profound 2. Zhang, S. et al. Proc. Natl Acad. Sci. USA http:// 10,11 dx.doi.org/10.1073/pnas.1523449113 (2016). siltstone holds trails of scratch marks, thought to change in the on Earth” . The 3. Sahoo, S. K. et al. (in the press). have been made by animals with exoskeletons, mat had previously covered the sea bed like a 4. Sperling, E. A. et al. Proc. Natl Acad. Sci. USA 110, walking on jointed legs — the earliest evidence coating of plastic wrap, leaving the underlying 13446–13451 (2013). 5. Wood, R. A. et al. Res. 261, 252–271 of arthropods in Earth’s history. sediments largely anoxic and off limits to - (2015). No one knows how much time passed in that mals. Because animals could not burrow deeply 6. Bengtson, S. & Zhao, Y. Science 257, 367–369 intervening rock — maybe as little as a few cen- in the Ediacaran, he says, “the mat meant that (1992). 7. Seilacher, A., Buatois, L. A. & Mángano, M. G. turies or millennia, says Narbonne. But during life was two-dimensional”. When grazing capa- Palaeogeog. Palaeoclimatol. Palaeoecol. 227, that short span, the soft-bodied, stationary Edi- bilities improved, animals penetrated the mat 323–356 (2005). acaran suddenly disappeared, driven to and made the sediments habitable for the first 8. Vannier, J., Calandra, I., Gaillard, C. & Zylinska, A. 38, 711–714 (2010). extinction by predators, he suggests. time, which opened up a 3D world. 9. Carbone, C. & Narbonne, G. M. J. Paleontol. 88, Narbonne has closely studied the few fauna Tracks from the early Cambrian show that 309–330 (2014). that survived this transition, and his findings animals started to burrow several centimetres 10. Mángano, M. G. & Buatois, L. A. Proc. R. Soc. B 281, 20140038 (2014). suggest that some of them had acquired new, into the sediments beneath the mat, which 11. Buatois, L. A., Narbonne, G. M., Mángano, M. C., more complex types of behaviour. The best clues provided access to previously untapped nutri- Carmona, N. B. & Myrow, P. Nature Commun. 5, come from traces left by peaceful, wormlike ents — as well as a refuge from predators. It’s 3544 (2014).

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