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Late Proterozoic Transitions in Climate, Oxygen, and Tectonics, and the Rise of Complex Life

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Late Proterozoic Transitions in Climate, Oxygen, and Tectonics, and the Rise of Complex Life LATE PROTEROZOIC TRANSITIONS IN CLIMATE, OXYGEN, AND TECTONICS, AND THE RISE OF COMPLEX LIFE NOAH J. PLANAVSKY1, LIDYA G. TARHAN1, ERIC J. BELLEFROID1, DAVID A. D. EVANS1, CHRISTOPHER T. REINHARD2, GORDON D. LOVE3, AND TIMOTHY W. LYONS3 1Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA <[email protected]> 2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA 30332, USA 3Department of Earth Sciences, University of California-Riverside, Riverside, CA 92521, USA ABSTRACT.—The transition to the diverse and complex biosphere of the Ediacaran and early Paleozoic is the culmination of a complex history of tectonic, climate, and geochemical development. Although much of this rise occurred in the middle and late intervals of the Neoproterozoic Era (1000–541 million years ago [Ma]), the foundation for many of these developments was laid much earlier, during the latest Mesoproterozic Stenian Period (1200–1000 Ma) and early Neoproterozoic Tonian Period (1000–720 Ma). Concurrent with the development of complex ecosystems, changes in continental configuration and composition, and plate tectonic interaction have been proposed as major shapers of both climate and biogeochemical cycling, but there is little support in the geologic record for overriding tectonic controls. Biogeochemical evidence, however, suggests that an expansion of marine oxygen concentrations may have stabilized nutrient cycles and created more stable environmental conditions under which complex, eukaryotic life could gain a foothold and flourish. The interaction of tectonic, biogeochemical, and climate processes, as described in this paper, resulted in the establishment of habitable environments that fostered the Ediacaran and early Phanerozoic radiations of animal life and the emergence of complex, modern-style ecosystems. INTRODUCTION diversification of eukaryotes, the earliest evidence for metazoan life, and dramatic reorganization of surface-ocean and benthic ecosystems and The late Proterozoic was witness to perhaps the environments. As such, this period likely provides most profound biological and geochemical an early glimpse of the regulatory feedbacks that, transition in Earth’s history. In contrast, the in the modern ocean, control the interactions preceding billion years appear to be characterized among organisms and biogeochemical cycling in by biogeochemical, climatic, and evolutionary Earth’s surface environments. Recent work also stasis. For example, there is little to no evidence suggests that this interval corresponded to a shift for continental ice sheets of any kind during this in the marine redox landscape, as well as surface- time interval (flippantly termed the “boring ocean oxygen levels (Lyons et al., 2014; Thomson billion”), suggesting climatic stability, and et al., 2014). Conventionally, Neoproterozoic unusually invariant carbon isotope data attest to oxygenation is considered to be a unidirectional the stability of the global carbon cycle. The late process, but it is likely that the Neoproterozoic, Proterozoic, in contrast, was characterized by and potentially even the early Paleozoic, were extreme biogeochemical and climatic volatility, as characterized by dynamic swings in oxygen recorded by pronounced and rapid variability in levels. the carbon isotope record and the stratigraphic The emerging view is that there are three record of repeated low-latitude glaciations of concurrent, but likely not coincidental, unparalleled scale and severity (Canfield, 2005; phenomena characterizing the early Lyons et al., 2012; Knoll, 2014). Moreover, the Neoproterozoic Earth system: 1) a shift in late Proterozoic records the evolution and ecosystem structure and function within the In: Earth-Life Transitions: Paleobiology in the Context of Earth System Evolution. The Paleontological Society Papers, Volume 21, P. David Polly, Jason J. Head, and David L. Fox (eds.). The Paleontological Society Short Course, October 31, 2015. Copyright © 2015 The Paleontological Society. PLANAVSKY ET AL.: LATE PROTEROZOIC RISE OF COMPLEX LIFE ocean, including the rise of eukaryotic algal the operation of eukaryote-driven processes. primary producers and the eventual emergence of Eukaryotic behavior, ranging from metazoan life; 2) severe low-latitude glaciation phytoplanktonic carbon fixation to filter-feeding, (the so-called ‘Snowball Earth’ events) and carnivory, bioturbation, and reef-building at carbon cycle instability; and 3) further and diverse scales and trophic levels, influences potentially dramatic oxygenation of Earth’s habitability and colonization. These relationships surface. The goal of this paper is to review the also shape sedimentological processes and timing and mechanistic relationships among these regulate biogeochemical cycling. In so doing, phenomena and to discuss our view of the eukaryotes mold the physical, chemical, and development and interaction of these factors may biotic landscape of both the benthos and the have shaped Earth’s environments and biosphere. surface ocean. As such, their appearance and We also hope to elucidate the role—if any—that radiation, which shifted the world’s oceans from a tectonic forcing may have played in controlling prokaryotic to eukaryotic mode, likely had a the observed Neoproterozoic biogeochemical concomitantly substantial impact upon transitions. An unusual concentration of environments as well as biogeochemical and continental area in the tropics is generally biotic processes (Fig. 1). Reconstructing the accepted to have been a key factor in the timing and nature of this transition, however, has development of extensive, ‘Snowball’-scale been limited by the ability to constrain the first glaciation. For example, a preponderance of appearance of the earliest eukaryotes and to track continental landmass at low latitudes would have their subsequent diversification—a task allowed for continued chemical weathering of the complicated by the likelihood that early continents, and thus extended carbon dioxide eukaryotic life was small, single-celled, and soft- drawdown, as the ice sheets advanced toward bodied. Efforts to reconstruct the early eukaryote lower latitudes. However, it is unclear if this record have been hampered by issues of both configuration was unique to the early preservation and recognition (Knoll, 2014). Neoproterozoic relative to the preceding billion However, recent efforts at improved sample years, and thus may have been only one of several collection, fossil detection and imaging, controlling factors. Finally, shifts in the flux of assessments of syngeity, and reconstruction of volcanogenic carbon dioxide or variations in the micro- and macro-scale taphonomic processes composition of the upper continental crust may (e.g., Javaux et al., 2004; Grey and Calver, 2007; have also been key contributing factors to the Anderson et al., 2014) are beginning to fill the climatic shifts recorded in the stratigraphic record gaps in the fossil record. The encouraging result is (Godderis et al., 2003; McKenzie et al., 2014), a clearer picture of early Earth ecosystems at the and further exploration of these ideas is essential dawn of eukaryotic life. in order to reconstruct the mechanisms that Historically, molecular-clock estimates for the regulated the biological, chemical, and physical origin of eukaryotes range widely from the dynamics of the Neoproterozoic world. Archean to the Paleoproterozoic, This paper reviews current records of late Mesoproterozoic, or even the Neoproterozoic Paleoproterozoic to early Neoproterozoic (1.8 Ga (e.g., Cavalier-Smith, 2002; Douzery et al., 2004; to 0.7 Ga) paleobiological diversity and Hedges et al., 2004; Yoon et al., 2004). The paleoecological complexity, marine redox molecular (biomarker) record of fossil lipids can, regimes, paleoclimate, atmospheric oxygen levels, in certain cases, fingerprint eukaryotes or even paleogeography, and crustal composition. We then particular eukaryotic clades. However, Archean explore relationships between these records and and Proterozoic biomarker data are susceptible to several Earth-system models that link climate, artifacts due to issues of high maturity and tectonics, and geochemical cycling to the initial contamination, and these factors need to be radiation of eukaryotes and complex ecosystems. assessed carefully. Rigorous self-consistency checks are needed to verify syngeneity of any THE RISE OF EUKARYOTES: THE organic compounds detected; thus, biomarker PROTEROZOIC FOSSIL RECORD evidence for eukaryotes other than from the youngest intervals of the Proterozoic has largely The composition, complexity, and distribution of been equivocal (e.g., Blumenberg et al., 2012; modern marine ecosystems are engineered Pawlowska et al., 2013; French et al., 2015). dramatically by the presence of eukaryotes and Efforts to differentiate early, single-celled 2 THE PALEONTOLOGICAL SOCIETY PAPERS, V. 21 FIGURE 1.—Approximate dates for the first appearance of various eukaryotic groups in the body fossil record (open black circles), the molecular fossil record (open blue circle), and best estimates from molecular clock techniques for the emergence of major crown groups (open red circles). Also shown are the fossils appearances of large ornamented Ediacaran microfossils (LOEMs) and vase shaped microfossils (VSMs). The vertical gray field denotes an interval of major eukaryotic diversification. After Planavsky et al. (2014). eukaryotes from prokaryotes in the body-fossil the evolutionary
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