Oxygen and Early Animal Evolution

Xiao, S. (2014). Oxygen and early animal evolution. In: J. Farquhar (ed.), Treatise on Geochemistry (2nd Edition), Volume 6: The Atmosphere -- History. Elsevier, Dordrecht. p. 231-250.

6.10

Oxygen and Early Animal Evolution

S Xiao, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA ã 2014 Elsevier Ltd. All rights reserved.

6.10.1 Introduction 6.10.2 Phylogenetic Context and Molecular Dating 6.10.2.1 Phylogenetic Topology 6.10.2.2 Molecular Dating 6.10.3 The Fossil Record of Early Metazoans 6.10.3.1 Pre-Ediacaran Record 6.10.3.1.1 Pre-Ediacaran metazoan trace fossils 6.10.3.1.2 Pre-Ediacaran metazoan body fossils 6.10.3.1.3 Pre-Ediacaran metazoan biomarkers 6.10.3.2 Ediacaran Record 6.10.3.2.1 Early Ediacaran Period 6.10.3.2.2 Late Ediacaran Period 6.10.3.3 Summary 6.10.4 Redox History of Ediacaran Oceans 6.10.5 Oceanic Oxygenation and Early Animal Evolution 6.10.5.1 General Considerations 6.10.5.2 Ecological and Genetic Factors 6.10.5.3 Oxygen and Animals: Distinguishing Chicken from Egg 6.10.6 Conclusion and Prospect Acknowledgments References

Glossary Acritarchs Organic-walled microfossils that cannot be easily classified into any modern group of organisms. Most acritarchs are resting cysts of phytoplankton, but some may be benthic organisms, some may represent actively growing rather than dormant stages, and some (such as Tianzhushania) may be animal diapause cysts. Bilaterians Bilaterally symmetric animals with body axes dividing their embryonic body into left and right, dorsal and ventral, and anterior and posterior parts. Bioturbation Disruption and mixing of sediments by organisms (mostly motile animals). Blastula Solid or hollow sphere of cells formed during an early embryonic stage in animal development through successive cleavages of a fertilized egg. Choanoflagellates Unicellular or colonial eukaryotes with a distinctive cell morphology characterized by an apical flagellum surrounded by a collar of microvilli. They are considered to be the closest living sister group to animals. Crown-group metazoans A monophyletic group that includes all living metazoans and their most recent common ancestor. Eumetazoans Animals characterized by tissue-grade differentiation into germ layers. Phylogenetically, living eumetazoans likely constitute a monophyletic group that includes cnidarians, ctenophores, and bilaterians, but excludes sponges. Mesozooplankton Planktonic animals (such as copepods) in the size range of 0.2–2 mm.

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Monophyletic group (clade) A group of taxa that consists of a common ancestor and all its descendants. Multicellularity Refers to multicelled organisms. The more advanced forms of multicellularity are characterized by cell differentiation and occur in animals, embryophytes, florideophyte red algae, laminarialean brown algae, ascomycete fungi, and basidiomycete fungi. Osmotrophy Acquiring nutrients through absorption or osmotic uptake of dissolved organic carbon across membranes or body surfaces. Paraphyletic group A group of taxa that consists of a common ancestor and some (but not all) of its descendants. Phylogenetics The determination of evolutionary relationships among taxa using morphological and molecular data, based on the principle that taxa sharing a common ancestor should also share one or more derived characters (synapomorphies). Phylogenomics refers to the use of genomic data to infer evolutionary relationships. Picoplankton Autotrophic or heterotrophic plankton in the size range of 0.2–2 mm. Placozoa An animal phylum characterized by a flat discoidal body plan with two epithelial layers enclosing a layer of multinucleate fiber cells. Only one living placozoan species has been described: Trichoplax adhaerens, which feeds through osmotrophy and phagocytosis. The Ediacaran organism Dickinsonia has been interpreted as a placozoan fossil. Rangeomorphs A group of Ediacaran fossils characterized by a modular and fractal-like body construction. These fossils typically consist of frondlets that are arranged in a repetitive, self-similar pattern. Examples include Rangea

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(Figure 4(b)) and Charnia. All rangeomorphs are extinct and they appear to be unique to the Ediacara biota. Stem-group metazoans Extinct lineages that lie phylogenetically outside the clade of crown-group metazoans but are more closely related to the crown-group animals than to any other living organisms. Stem-group

6.10.1

Introduction

Although oxygen is the third most abundant element in the universe, molecular dioxygen (O2, referred to as oxygen in this chapter for simplicity) does not exist in much abundance due to its high reactivity. Indeed, an exceptional abundance of atmospheric O2 makes the planet unique and, because it requires a strong biological source, may be regarded as a biosignature for an active biosphere in astrobiological search (Le´ger et al., 2011). On Earth, the abundance of O2 has transformed the biosphere and allowed for the evolution of complex life (such as animals) with macroscopic size and energetically expensive metabolism (Catling et al., 2005; Decker and van Holde, 2011; Raff and Raff, 1970; Runnegar, 1982b) largely because the reduction of O2 coupled with the oxidation of organic carbon yields copious free energy to support metabolism and growth. Not surprisingly, therefore, the radiation of animals is often hypothesized to have been triggered by the rise of O2 levels in the atmosphere and oceans, perhaps in the Ediacaran Period (635–542 Ma) (Berkner and Marshall, 1965; Cloud, 1968; Knoll, 2003; Nursall, 1959). This hypothesis, however, is remarkably difficult to test largely because the O2 level in ancient atmosphere and oceans is difficult to quantify, the divergence time of various animal clades is poorly constrained, the phylogenetic affinity of early animal fossils is difficult to ascertain, and the physiology of early animals is often unknown. As will become clear later, this hypothesis also suffers from the often vague definition of animals, as different animal groups are expected to have different levels of oxygen demand depending on their specific physiology and metabolism. At a different level, even if a temporal linkage is established, a causal linkage can be difficult to ascertain. Specifically, because of the possible two-way interactions between animals and oceanic redox conditions, it can be difficult to distinguish whether oxygenation was a cause or consequence of animal evolution. Despite these difficulties, however, phylogeneticists, paleobiologists, and geochemists have generated a tremendous amount of data in recent decades that begin to illuminate the murky history of early animal evolution and oceanic oxygenation. In this chapter, the author presents a review of the newly published data, with a focus on the Ediacaran Period.

6.10.2 6.10.2.1

Phylogenetic Context and Molecular Dating Phylogenetic Topology

Phylogenetic relationships can be inferred from morphological and molecular data based on the concept of synapomorphy (shared derived character). With increasingly available genetic

metazoans always lack one or more features that collectively define crown-group metazoans. Syncytiality Refers to large cells filled with cytoplasm and containing multiple nuclei. Taphonomy Study of the degradation, burial, diagenesis, and formation of fossils.

and genomic data, as well as improved bioinformatics algorithms and sequence evolution models, phylogenetic hypotheses have been put to rigorous tests (Dunn et al., 2008; Kocot et al., 2011; Philippe et al., 2011a; Sperling et al., 2009; Srivastava et al., 2008, 2010). There has been some broad consensus about the basic topology of the animal phylogenetic tree (Figure 1): (1) Animals are monophyletic; (2) choanoflagellates are the closest living relatives of animals; (3) bilaterians are monophyletic; and (4) bilaterians consist of three supraphylum-level clades – ecdysozoans, lophotrochozoans, and deuterostomes. In addition, the following features have been recovered in many phylogenetic analyses, although dissenting opinions have been published: (1) Eumetazoans are often resolved as a monophyletic group (but see Dunn et al., 2008); (2) sponges are paraphyletic at the base of the animal phylogenetic tree (but see Botting et al., 2012; Philippe et al., 2009); and (3) the placozoan Trichoplax adhaerens forms a sister group to the eumetazoans (but see Schierwater et al., 2009). Finally, some long-held phylogenetic concepts have been questioned by molecular phylogeneticists. An example more relevant to the discussion is acoelomorph flatworms, which have been traditionally regarded as basal bilaterian animals – an interpretation supported by their morphological simplicity and which enjoys some molecular phylogenetic support (Ruiz-Trillo et al., 1999; Telford et al., 2003). But the basal bilaterian interpretation was probably due to the morphological reduction of acoelomorphs and a phylogenetic artifact known as long-branch attraction, and renewed analyses indicate that they may be morphologically simplified deuterostomes (Erwin et al., 2011; Philippe et al., 2011b). The topology of animal phylogeny allows one to make inferences about the body plan complexity of early animals, based on the principle of parsimony (Erwin, 2006). For example, all living animals are characterized by obligate multicellularity with functional cell adhesion proteins, cell differentiation, and programmed cell death, whereas living choanoflagellates are unicellular or colonial even if they may express genes coding for proteins involved in animal cell interactions (King et al., 2003). Thus, the phylogenetic tree shown in Figure 1 implies that the last common ancestor of living animals must have been multicellular. It follows that (1) the first stem-group animals that diverged from choanoflagellates could in principle be unicellular, microscopic, and morphologically simple; (2) a series of genomic evolutionary events leading to animal multicellularity must have occurred along the stem of metazoans; and (3) these events should be recorded in extinct stem-group metazoans (Marshall and Valentine, 2010). As another example, nerve systems, digestive systems, and muscle cells are found in all living (crown-group) eumetazoans but not in sponges or placozoans. Thus, these features probably did not exist in the last common


Stage 5 Stage 4 Stage 3 Stage 2

Fortunian

Avalon Assm.

580 600

Cnidaria Rise of macroscopic, motile, actively feeding, high O2 demanding animals?

Early

Nama Assm. White Sea Assm.

560

Arthropoda

Priapulida

Bryozoa

Annelida

Mollusca

Nemertea

Vertebrata

Echinodermata

Hemichordata

Placozoa

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Ordovician

540

Ediacaran

Millions of years before present

520

Ecdysozoans

Middle

Terrenuvian Series 2

500

Phanerozoic

480

Cambrian

460

Demospongiae

Choanoflagellata

Deuterostomes

Brachiopoda

Eumetazoans Bilaterians Lophotrochozoans

Onychophora

Sponges

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Gaskiers glaciation

620 Marinoan glaciation

640 660

Dominated by microscopic, or sessile, passively feeding, low O2 demanding animals?

720

Cryogenian

700

Neoproterozoic

680

Sturtian glaciation

740 760 780

Phyla Classes

800

Stem groups Ediacaran genera

850

Crown-group estimates 900

Tonian

Known stratigraphic range – macrofossils Known stratigraphic range – biomarkers

950

Potential range extension

1000

0

20

40

60

80

100

120

140

Figure 1 Animal phylogeny, molecular dating, fossil record, and oxygen demand. Phylogenetic tree shows evolutionary relationships of major phylumlevel taxa, with omissions of several important animal groups (e.g., ctenophores and acoelomorph flatworms) whose phylogenetic positions are controversial. Supraphylum clades are marked as labeled, horizontal, black bars. Estimated crown-group divergence time (i.e., last common ancestor of living representatives) of major phyla is shown in colored dots. Fossil record of animal phyla is marked as vertical bars (black, macrofossils; gray, biomarkers; and white, potential range extension). Fossil diversity is shown as horizontal histogram (scale at bottom: blue, Cambrian–Ordovician animal phyla; yellow, Cambrian–Ordovician animal classes; and green, Ediacara macrofossil genera, with microfossils and macroalgae excluded). Thick vertical bar in gray-black to the right denotes phylogenetic, physiological, and redox transitions from early Neoproterozoic to late Ediacaran. Modified from Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, and Peterson KJ (2011) The Cambrian conundrum: Early divergence and later ecological success in the early history of animals. Science 334: 1091–1097.

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ancestor of animals, but evolved after the placozoan–eumetazoan divergence and along the stem toward the eumetazoans. Using the same principle of parsimony, one can infer the ecology of early animals, including their feeding strategies and physiologies (Erwin et al., 2011; Sperling and Vinther, 2010). Importantly, living sponges are sessile microphagous or osmotrophic feeders; sponge choanocytes lining a water canal system trap bacteria and absorb dissolved organic carbon from water currents (Sperling et al., 2007), a feeding strategy similar to that of choanoflagellates except that the feeding cells in sponges are more organized and better coordinated. T. adhaerens also feeds through osmotrophy or phagocytosis (Sperling and Vinther, 2010; Srivastava et al., 2008). Thus, the phylogenetic topology of Figure 1 implies that early animals (including stem-group animals phylogenetically positioned between the animal–choanoflagellate divergence and crown-group animals, as well as sponge- and placozoan-grade animals) may have fed microphagously or osmotrophically, a feeding mode that requires relatively low oxygen and energy demands. All living eumetazoans are characterized by a digestive system with a gut and are macrophagous feeders. Thus, it is a reasonable assumption that the last common ancestor of crown-group eumetazoans was also a macrophagous feeder (Peterson and Butterfield, 2005; Peterson et al., 2005). Most bilaterians are motile animals, and their body plan with anterior–posterior differentiation is an adaptation for directional locomotion. Hence, it is likely that the last common ancestor of crowngroup bilaterians was a mobile animal that required more oxygen and energy demands than sponge-grade animals. Finally, phylogenetic considerations suggest that early bilaterians were probably filter- or detritus-feeders and that the energetically more demanding feeding strategy – carnivorous predation that involves actively pursuing a prey – is a phylogenetically derived feature in lophotrochozoans, ecdysozoans, and deuterostomes (Erwin et al., 2011). Thus, phylogenetic topology predicts that early animals successively progressed from microscopic to macroscopic size, from sessility to motility, and from passive to active feeding modes – a progression that demands successively greater oxygen levels.

crown groups diverged near the Ediacaran–Cambrian boundary (Figure 1). Combining the molecular clock estimates with the phylogenetic inferences of early animal ecology, it can be argued that the Cryogenian or pre-Cryogenian animals were probably dominated by osmotrophic and microphagous feeders that demanded relatively low levels of oxygen. More active and oxygen-demanding feeding strategies evolved later, during the Ediacaran and Cambrian periods. This argument, based on phylogenetic and molecular clock data, provides a framework independent of the fossil record to evaluate the possible temporal and causal relationship between oxygenation and animal evolution. As will become clear in the succeeding text, it is assuring that the phylogenetic inferences are broadly in congruence with the fossil record, which shows that sessile osmotrophic or microphagous stem-group and crown-group animals were probably dominant up until the middle Ediacaran Period (Clapham et al., 2003; Laflamme et al., 2009; Sperling and Vinther, 2010; Xiao and Laflamme, 2009), whereas motile and actively feeding animals became more prominent toward the late Ediacaran and early Cambrian periods (Bush et al., 2011; Dunne et al., 2008; Erwin et al., 2011; Xiao and Laflamme, 2009).

6.10.3 6.10.3.1

The Fossil Record of Early Metazoans Pre-Ediacaran Record

One of the greatest challenges in the study of Proterozoic animal fossils is to establish their metazoan affinity. This is not a simple task because many of these fossils are morphologically simple, and thus diagnostic features are few. Nonetheless, there have been numerous reports of pre-Ediacaran animal fossils dating back to the Paleoproterozoic. Runnegar and Fedonkin (1992) and Fedonkin and Runnegar (1992) provided reviews of Proterozoic metazoan body and trace fossils, respectively, and discounted most pre-Ediacaran metazoan fossils as pseudofossils or dubiofossils, an assessment that has also been reached by others (Cloud, 1968; Jensen et al., 2005, 2006).

6.10.3.1.1 Pre-Ediacaran metazoan trace fossils 6.10.2.2

Molecular Dating

There have been many attempts to date the evolutionary history of animals (Blair, 2009; Erwin et al., 2011; Peterson et al., 2004; Runnegar, 1982a; Wray et al., 1996), and the results vary widely. For example, the last common ancestor of living animals has been estimated at 1200 Ma (Wray et al., 1996), 653 Ma (Peterson et al., 2004), 664 Ma (Peterson and Butterfield, 2005), 766 Ma (Peterson et al., 2008), and 784 Ma (Erwin et al., 2011). These molecular dates come with large uncertainties, but more recently published dates point to a Cryogenian origin of crown-group animals. This implies that stem-group animals could have existed in the pre-Cryogenian time. However, considering that the last common ancestor of choanoflagellates and animals arose 10% PAL) or an active circulatory system (possibly with oxygen transport proteins such as hemoglobin, hemocyanin, and hemerythrin) to distribute oxygen throughout their tissues (Decker and van Holde, 2011). Such Ediacaran organisms include the White Sea fossil Kimberella (Figure 4(d)) that was an actively motile bilaterian grazer with a thickened dorsal shield (Fedonkin et al., 2007a; Ivantsov, 2009), numerous animals that left burrowing traces in Ediacaran sediments (Chen et al., 2013; Jensen et al., 2005), and Cloudina that had a mineralized tube and was probably

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preyed upon by other predatorial animals (Bengtson and Yue, 1992; Hua et al., 2003). If one assumes that a threshold pO2 level of 10% PAL is needed for the evolution of macroscopic eumetazoans, when was the threshold crossed? This question needs to be answered to establish or falsify a causal relationship between oxygen and animal evolution. Many Cryogenian basins are characterized by anoxic and often sulfidic conditions (Canfield et al., 2008; Dahl et al., 2010; Johnston et al., 2010; Li et al., 2012; Poulton and Canfield, 2011; Scott et al., 2008), sometimes even within the oceanic mixed layer (Johnston et al., 2010). Gaidos (2011) estimated that the persistent presence of sulfidic conditions in the oceanic mixed layer would limit atmospheric pO2 levels to 150–200 mM (or atmospheric pO2 levels of 46–62% PAL) are required to maintain even minimally aerobic deep-ocean conditions, given phosphorus availability of 0.91 mM to drive primary production in surface waters. Thus, Ediacaran atmospheric pO2 levels were probably between 4 and 46% PAL, if anoxia but not euxinia was prevalent in Ediacaran deep waters. Despite anoxia in Ediacaran deep basins, Mo concentrations and Mo isotopes point to episodes of global oxygenation of deep oceans and hence an increase in atmospheric pO2 levels in the late Ediacaran ( d34SCAS) in the terminal Proterozoic Nama Group, southern Namibia: A consequence of low seawater sulfate at the dawn of animal life. Geology 37: 743–746. Rothman DH, Hayes JM, and Summons R (2003) Dynamics of the Neoproterozoic carbon cycle. Proceedings of the National Academy of Sciences of the United States of America 100: 8124–8129. Ruiz-Trillo I, Riutort M, Littlewood DTJ, Herniou EA, and Baqun˜a J (1999) Acoel flatworms: Earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283: 1919–1923. Runnegar B (1982a) A molecular-clock date for the origin of the animal phyla. Lethaia 15: 199–205. Runnegar B (1982b) Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of the burrowing habit. Alcheringa 6: 223–239. Runnegar B (1991) Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes. Palaeogeography, Palaeoclimatology, Palaeoecology 97: 97–111. Runnegar BN and Fedonkin MA (1992) Proterozoic metazoan body fossils. In: Schopf JW and Klein C (eds.) The Proterozoic Biosphere: A Multidisciplinary Study, pp. 369–388. Cambridge: Cambridge University Press. Sahoo SK, Planavsky NJ, Kendall B, et al. (2012) Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489: 546–549. Schierwater B, Eitel M, Jakob W, et al. (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern ‘urmetazoon’ hypothesis. PLoS Biology 7(1): e1000020. Schiffbauer JD, Xiao S, Sen Sharma K, and Wang G (2012) The origin of intracellular structures in Ediacaran metazoan embryos. Geology 40: 223–226. Schopf KM and Baumiller TK (1998) A biomechanical approach to Ediacaran hypotheses: How to weed the Garden of Ediacara. Lethaia 31: 89–97. Schro¨der S and Grotzinger JP (2007) Evidence for anoxia at the Ediacaran-Cambrian boundary: The record of redox-sensitive trace elements and rare earth elements in Oman. Journal of the Geological Society 164: 175–187. Scott C, Lyons TW, Bekker A, et al. (2008) Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452: 456–459. Seilacher A (2007) Trace Fossil Analysis. Berlin: Springer. Seilacher A, Bose PK, and Pflu¨ger F (1998) Triploblastic animals more than one billion years ago: Trace fossil evidence from India. Science 282: 80–83. Seilacher A, Buatois LA, and Ma´ngano MG (2005) Trace fossils in the Ediacaran– Cambrian transition: Behavioral diversification, ecological turnover and environmental shift. Palaeogeography, Palaeoclimatology, Palaeoecology 227: 323–356. Sergeev VN, Knoll AH, and Vorob’Eva NG (2011) Ediacaran microfossils from the Ura Formation, Baikal-Patom Uplift, Siberia: Taxonomy and biostratigraphic significance. Journal of Paleontology 85: 987–1011. Servais T, Lehnert O, Li J, et al. (2008) The Ordovician Biodiversification: Revolution in the oceanic trophic chain. Lethaia 41: 99–109. Sharma M and Shukla Y (2012) Megascopic carbonaceous compression fossils from the Neoproterozoic Bhima Basin, Karnataka, South India. In: Bhat GM, Craig J, Thurow JW, Thusu B, and Cozzi A (eds.) Geology and Hydrocarbon Potential of

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