Coupling of ocean redox and animal evolution during the Ediacaran-Cambrian transition

Wang, Dan; Ling, Hong‐Fei; Struck, Ulrich; Zhu, Xiangkun; Zhu, Maoyan; He, Tianchen; Yang, Ben; Gamper, Antonia; Shields, Graham A.

doi:10.1038/s41467-018-04980-5

Cited by 83 publications

(44 citation statements)

References 68 publications

(115 reference statements)

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“…However, it remains unclear as to whether animal diversification and increased ecosystem complexity was driven extrinsically by the expansion of permissive oxic niches, or by genetic or developmental innovations that enabled animals to expand into the oxic realm. These dynamic carbon and redox records are also closely tied to probable changes in nutrient cycling, but mechanistic details are far from clear (15,20,48,49). For example, step changes in the burial of phosphorus and organic carbon, driven by evolutionary innovations, have been argued to have progressively lowered marine phosphate concentrations (15).…”

Section: Biotic Response To Changing Redox: a Role For Instability?mentioning

confidence: 99%

Integrated records of environmental change and evolution challenge the Cambrian Explosion

et al. 2019

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The 'Cambrian Explosion' describes the rapid increase in animal diversity and abundance, as manifest in the fossil record, between ~ 540 and 520 million years ago (Ma). This event, however, is nested within a far more ancient record of macrofossils extending at least into the late Ediacaran, ~571 Ma. The evolutionary events documented during the Ediacaran-Cambrian interval coincide with geochemical evidence for the modernisation of Earth's biogeochemical cycles. Holistic integration of fossil and geochemical records leads us to challenge the notion that the Ediacaran and Cambrian worlds were markedly distinct, and places biotic and environmental change within a longer-term narrative. We propose that the evolution of metazoans may have been facilitated by a series of dynamic and global changes in redox conditions and nutrient supply, which, together with potential biotic feedbacks, enabled turnover events that sustained phases of radiation. In this synthesis, we argue that early metazoan diversification should be recast as a series of successive, transitional radiations that extended from the late Ediacaran and continued through the early Palaeozoic. We conclude that while the Cambrian Explosion represents a radiation of crown-group bilaterians, it was simply one phase amongst several older, and younger, metazoan radiations.

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Section: Biotic Response To Changing Redox: a Role For Instability?mentioning

confidence: 99%

Integrated records of environmental change and evolution challenge the Cambrian Explosion

et al. 2019

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“…High seafloor O 2 fugacity during the deposition of the Shibantan limestone seems contradictory with the modest atmospheric p O 2 levels and extensive seafloor anoxia in Ediacaran and Cambrian 8,59 . Local seafloor oxygenation must require a continuous O 2 supply to maintain oxic status under such predominately anoxic condition.…”

Section: Discussionmentioning

confidence: 97%

Early animal evolution and highly oxygenated seafloor niches hosted by microbial mats

Ding

Dong

Sun

et al. 2019

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The earliest unambiguous evidence for animals is represented by various trace fossils in the latest Ediacaran Period (550–541 Ma), suggesting that the earliest animals lived on or even penetrated into the seafloor. Yet, the O2 fugacity at the sediment-water interface (SWI) for the earliest animal proliferation is poorly defined. The preferential colonization of seafloor as a first step in animal evolution is also unusual. In order to understand the environmental background, we employed a new proxy, carbonate associated ferrous iron (Fecarb), to quantify the seafloor oxygenation. Fecarb of the latest Ediacaran Shibantan limestone in South China, which yields abundant animal traces, ranges from 2.27 to 85.43 ppm, corresponding to the seafloor O2 fugacity of 162 μmol/L to 297 μmol/L. These values are significantly higher than the oxygen saturation in seawater at the contemporary atmospheric pO2 levels. The highly oxygenated seafloor might be attributed to O2 production of the microbial mats. Despite the moderate atmospheric pO2 level, microbial mats possibly provided highly oxygenated niches for the evolution of benthic metazoans. Our model suggests that the O2 barrier could be locally overcome in the mat ground, questioning the long-held belief that atmospheric oxygenation was the key control of animal evolution.

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“…The latter is revealed by the inter-regional (gamma)-diversity peak reflecting formation of numerous isolated faunal provinces2. By contrast, minor extinction events here and elsewhere appear to be associated with the negative excursions11,18,46. In the deeper ocean setting of northern Siberia and South China, multi-proxy analyses reveal broadly similar oceanic redox fluctuations4,47–49, which coincide with the positive carbon isotope excursions in the early Cambrian16,46,50.…”

Section: Environmental Oxygenation and Animal Radiationsmentioning

confidence: 91%

Possible links between extreme oxygen perturbations and the Cambrian radiation of animals

et al. 2019

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The role of oxygen as a driver for early animal evolution is widely debated. During the 21 Cambrian explosion, episodic radiations of major animal phyla occurred coincident with 22 repeated carbon isotope fluctuations. However, the driver of these isotope fluctuations and 23 potential links to environmental oxygenation are unclear. Here, we report high-resolution 24 carbon and sulphur isotope data for marine carbonates from the southeastern Siberian 25 Platform that document the canonical explosive phase of the Cambrian radiation from ~524 26 to ~514 Myr ago. These analyses demonstrate a strong positive covariation between 27 carbonate  13 C and carbonate-associated sulphate  34 S through five isotope cycles. 28 Biogeochemical modelling suggests that this isotopic coupling reflects periodic oscillations 29 in atmospheric O2 and the extent of shallow ocean oxygenation. Episodic maxima in the 30 biodiversity of animal phyla directly coincided with these extreme oxygen perturbations. 31 Conversely, the subsequent Botoman Toyonian animal extinction events (~514 to ~512 32Myr ago) coincided with decoupled isotope records that suggest a shrinking marine 33 sulphate reservoir and expanded shallow marine anoxia. We suggest that fluctuations in 34 oxygen availability in the shallow marine realm exerted a primary control on the timing and 35 tempo of biodiversity radiations at a crucial phase in the early history of animal life. 36 37The early Cambrian witnessed a dramatic diversification of animal body plans and 38 behaviours 1 , as well as between-species interactions and palaeocommunity innovations 2,3 , 39 ultimately leading to modern animal ecosystems. Ocean oxygenation is a commonly invoked 40 environmental pre-requisite 4 6 . However, some recent studies suggest that despite probable 41 low-oxygen conditions, the oceans exceeded requisite oxygen thresholds for simple animals, 42 such as sponges, well before the Cambrian Period 7,8 . Many of the new animal body plans and 43 lifestyles that appeared during the early Cambrian were associated with considerably higher 44 oxygen demands 9,10 . Fluctuations in the maximum dissolved oxygen content of surface 45 waters, or the extent of shallow ocean oxygenation, could therefore have played an important 46 role in regulating the pattern of Cambrian radiations. This brings into question the role of 47 55 single, large oxidised oceanic reservoir (dissolved sulphate and inorganic carbon), the isotopic 56 composition of which is governed by isotope fractionation during microbially-mediated 57 reduction to sulphide (ultimately preserved as pyrite) and organic carbon. Burial of these 58 reduced species represents the two main net sources of oxygen to the surface environment 12 59 14 , and also imprints on both the seawater sulphate sulphur isotope ( 34 S, as recorded by 60 carbonate-associated sulphate) and carbon isotope ( 13 C, as recorded in carbonate) records, 61 allowing redox changes in the surface environment to be traced through geologic time.62 63 Here we present...

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Coupling of ocean redox and animal evolution during the Ediacaran-Cambrian transition

Cited by 83 publications

References 68 publications

Integrated records of environmental change and evolution challenge the Cambrian Explosion

Integrated records of environmental change and evolution challenge the Cambrian Explosion

Early animal evolution and highly oxygenated seafloor niches hosted by microbial mats

Possible links between extreme oxygen perturbations and the Cambrian radiation of animals

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