Geobiology (2003), 1, 3 – 14

The geological consequences of evolution
Geological L A R T I C L E O R I G I N Publishing Ltd. Blackwell Aconsequences of evolution

A ND R E W H . K N O L L Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA

ABSTRACT
Geobiologists seek to understand the role of organisms in the Earth system. By extension, one can ask how evolutionary innovations and, more generally, the population genetic processes that mediate evolution have influenced the Earth’s surface through time. The example of oxygenic photosynthesis and the redox history of atmospheres and oceans illustrates the complex relationship between evolution and environmental change. Biological innovations determine the dimensions of biological participation in the Earth system, but by themselves they seldom generate lasting environmental change. More commonly, environments change when physical drivers exceed the limited environmental buffering capacity conferred by population genetics and nutritional codependence. Environmental change, in turn, feeds back on biology, creating new opportunities for evolutionary innovation. Received 05 December 2002; accepted 05 February 2003 Corresponding author: Professor Andrew H. Knoll. Tel.: 001 617 495 9306; e-mail: aknoll@oeb.harvard.edu

INTRODUCTION
Geobiology is widely appreciated as a new enterprise within the Earth sciences. It may therefore come as a surprise that the founding document of geobiological thought is none other than the foundational text of modern geology, James Hutton’s (1788) Theory of the Earth. Much as Charles Darwin (1859) did in The Origin of Species, Hutton carefully documented what he saw around him – commonly, quotidian observations that anyone might have made. But, again like Darwin, Hutton marshalled his observations in support of a sophisticated and, in its time, revolutionary worldview. Hutton’s arguments strike the 21st century reader as surprisingly modern, but then our sense of modernity in geological thought derives in no small measure from Hutton himself. Hutton explicitly asked how the Earth can maintain itself as a habitable planet. In true late eighteenth century fashion, he observed that the distribution of land and sea provides habitats well suited for plants and animals. Hutton also noted, however, that erosion inexorably if slowly wears down the land, while sediments supplied by rivers continually fill in the sea. How then can the Earth continue in the long term as an abode for life? Hutton recognized that sustained habitability cannot depend on environmental stasis, because the land and sea are demonstrably not static. One further observation, however, suggested an alternative explanation. Sedimentary rocks in the hills and mountains of Scotland contain the fossilized shells of marine animals, prompting Hutton to conceive of a world in
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which the consolidation and uplift of marine sediments (driven, in his view, by heat) completed a cycle that linked erosion and deposition. Habitats for plants and animals were maintained dynamically by what Hutton (1785) called the System of the Earth. Interestingly, despite Hutton’s biological motivation, life contributes little in the way of process to the dynamics of his Earth system. As Lovelock (1989) has observed, Hutton did liken the Earth to a superorganism, but taken in context, this has to be understood as metaphor, not archae-cybernetics – Hutton’s imagery did not imply that biological physiology contributed substantially to geophysiology. There is passing acknowledgement that plants may speed erosion by contributing to the breakup of rocks, but in general life is simply served by a physical system. The idea that life itself constitutes a suite of geologically important processes is much more recent, surfacing early in the last century in the writings of Vernadsky (1926) and, more recently (and famously), in James Lovelock’s (1979) conception of Gaia. Of course, Gaia itself sometimes seems to be suspended uncomfortably between metaphor and systems science. As research focuses ever more resolutely and with increasing maturity on the Earth system, it is useful to ask what roles are played by the system’s constituent parts, and how changes in individual parts may influence the system as a whole. That is the nature of the question I wish to explore in this essay. I will not consider in detail whether or how biological processes contribute to the maintenance of the Earth system – it is well understood that they do, and many scientists have 3

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ANDREW H. KNOLL parent (bacterio)chlorophyll and gets passed in bucket brigade fashion through a chain of redox reactions, eventually to drive formation of reducing power in the form of NADPH and chemical energy, as ATP. The electron transport chain can be cyclic – that is, the electron, stripped of its energy, can be returned to the reaction centre. Or it can be non-cyclic, in which case a new electron must be found to restore the reaction centre pigment (see Falkowski & Raven, 1997, for a thorough review of light reactions in photosynthesis). Most photosynthetic bacteria have a single photosystem linked to an electron transport chain containing either Fequinones or Fe–S proteins. Electron resupply comes from = H2S, S2O3 , H2, organic molecules, or even Fe2+, and oxygen does not enter the picture. Cyanobacteria are unique among photosynthetic bacteria because they contain two coupled photosystems. H2O provides the electrons needed for photosynthesis, and O2 is generated as a by-product. Interestingly, in cyanobacteria, the coupled photosystems differ from one another: photosystem II contains Fe-quinones, like those of proteobacteria and green non-sulphur bacteria, whereas photosystem I uses Fe–S proteins like those of green sulphur bacteria and heliobacteria. This suggests that cyanobacterial photosynthesis, with its capacity for oxygen generation, evolved from pre-existing anoxygenic phototrophs by lateral transfer of a photosystem gene cassette (Blankenship, 1992). Of course, more than lateral transfer was needed to assemble the two photosystems coupled in cyanobacteria. Oxygenic photosynthesis required reaction centre molecules with a standard potential sufficient to drive the oxidation of water – a good case can be made for the evolution of chlorophyll a from bacteriochlorophyll g, found in the closely related heliobacteria (Kobayashi et al., 1998). It also required the evolution of a molecular complex at the front end of photosystem II that can bind H2O and extract the electrons needed to replace those lost by photon excitation. Buchel et al. (1999) have recently proposed that a manganese bicarbonate complex originally provided electrons for photosynthesis, eventually giving rise to the Mn-catalysed protein complex that splits water to produce both electrons and oxygen in present-day cyanobacteria. Finally, an entirely different set of reactions was needed – the so-called ‘dark reactions’ that fix carbon dioxide to form sugar, using the ATP and reducing power generated by light reactions. Carbon fixation in cyanobacteria proceeds via the familiar Calvin–Benson cycle, as it does in photosynthetic proteobacteria. Other photosynthetic bacteria, however, employ quite different molecular pathways to fix CO2 (Fuchs & Stupperich, 1985). The preceding comments only hint at the molecular complexity of photosynthesis, but they suffice to show that oxygenic photosynthesis is an intricate construction that unites several distinct molecular innovations to form a unique functional system. From an ecological perspective, this concatenation might well be regarded as the central event in the history of life, because it liberated biology from hydrothermal vents
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contributed to the elucidation of the mechanisms by which this occurs. Rather, I wish to ask a subtly different question: How and to what extent have processes of evolution contributed to the changing state of Earth surface environments? The fact that biology participates significantly in the Earth system does not necessarily mean that biological evolution drives environmental change through time. I will focus on one example, the evolution of oxygenic photosynthesis, that exemplifies how evolutionary innovations inferred from comparative biology and planetary history drawn from palaeontology and geochemistry can illuminate some principal issues in geobiology. I choose this example because the supporting facts are reasonably well known (if not universally agreed upon), increasing, I hope, the transparency of the approach I wish to illustrate. I will also consider, at least briefly, whether the mechanistic processes of evolutionary biology – principally those of population genetics – generally contribute to change or stasis in the Earth system.

THE EVOLUTION OF PHOTOSYNTHESIS AND ITS GEOBIOLOGICAL CONSEQUENCES
If there is one fact that every geophysicist knows about biology it is that photosynthesis generates the oxygen that makes air breathable. At one level, this observation is indisputable – in the absence of oxygenic photosynthesis Earth’s atmosphere could not contain 21% O2 by volume, and were oxygenic photosynthesis to be suspended, the atmospheric reservoir of oxygen would decay over an interval of several million years. But let us ask two slightly different questions. (1) What is the historical relationship between the evolutionary innovation of oxygenic photosynthesis and the changing redox state of the atmosphere and oceans? Was the oxidation of the biosphere the inevitable and immediate consequence of photosynthetic innovation, or is there more at issue? (2) To the extent that evolution and environmental history are linked, does the vector of causation run in only one direction? Or, has atmospheric change itself influenced the continuing evolution of photosynthetic organisms? The biology of photosynthesis First, we must understand the biological innovation in question. It was not the evolution of photosynthesis. The use of solar energy to drive the reduction of carbon dioxide and generate ATP evolved early within the bacteria. At least five major bacterial clades (cyanobacteria, proteobacteria, heliobacteria, green sulphur bacteria, and green non-sulphur bacteria) include photosynthetic organisms, and four of these do not produce oxygen as a by-product (Blankenship, 1992). In all photosynthetic bacteria, pigments (chlorophyll or bacteriochlorophyll, plus accessory pigments) absorb photons of light. Within the photosynthetic reaction centre, each photon’s energy is transferred to an electron, which leaves its

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Fig. 1 Proterozoic microfossils reliably interpreted as cyanobacteria. (A) Eohyella, a fossil counterpart of the extant endolithic cyanobacterium Hyella, preserved in silicified ooids from the Neoproterozoic Limestone–Dolomite Series, East Greenland; (B) A species of the modern cyanobacterial genus Entophysalis, from Shark Bay, Australia, for comparison with C (photo by John Bauld). (C) Eoentophysalis, a mat-forming colonial cyanobacterium from silicified tidal flat carbonates of the early Mesoproterozoic Bil-yakh Group, northern Siberia. (D) Polybessurus, fossil counterpart of extant Cyanostylon-like cyanobacteria, preserved in silicified tidal flat carbonates from the Neoproterozoic Draken Formation, Spitsbergen. Scale bars in B = 125 µm for A, and 30 µm for B–D.

and other environments where locally strong redox gradients could support chemosynthetic life, allowing organisms to spread across the planet (Knoll & Bauld, 1989). And it only happened once. The ‘green-plant’ photosynthesis found in algae and land plants is explained by another form of lateral transfer – the incorporation into eukaryotes of entire cyanobacterial cells (Margulis, 1981; Delwiche, 1999). The antiquity of oxygenic photosynthesis Did the innovation of oxygenic photosynthesis translate directly and immediately into an oxic atmosphere and oceans? To address this, we must ask palaeontologists when cyanobacteria evolved, and compare that estimate with the history of atmospheric oxygen inferred from geochemical proxies.
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The palaeobiological question is: how can we identify a cyanobacterial signature in sedimentary rocks? Microfossils provide an obvious means of addressing this question. In terms of morphology, cyanobacteria are among the most diverse of all bacteria, and while some cyanobacteria are simple and have forms replicated widely among bacteria, others have morphologies not known in other bacterial clades (Geitler, 1930–1932). Thus, the distinctive morphology and behaviour of endoliths such as Hyella is unambiguous when observed in Proterozoic fossils from East Greenland (Green et al., 1988; Fig. 1A). The same is true of the cushions of stalked Cyanostylon-like fossils commonly found in chert nodules within Neoproterozoic tidal flat carbonates (Green et al., 1987; Fig. 1D). The oldest fossils that have a morphology diagnostic for cyanobacteria are Entophysalis-like colonies preserved in

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ANDREW H. KNOLL that observed fractionation records the additive efforts of carbon fixation by the reductive citrus acid cycle (8–12‰) and secondary fractionation associated with methanogenesis and methanotrophy (Knoll & Canfield, 1998). Indeed, recent reinterpretations of reduced carbon in Early Archean rocks raise the spectre that non-biological C-isotopic fractionation might have been important on the early Earth. C-isotopic fractionation associated with Fischer–Tropsch and other abiological processes tends to be strongly condition dependent (Chang et al., 1983). In consequence, varying concentrations of reactants might lead to variable δ13Corg where abiological processes were prominent parts of the carbon cycle. Graphite from phosphate granules in the ∼ 3.8 Ga Akilia gneisses of south-western Greenland varies by as much as 40‰ (Mozjsis et al., 1996; see also Van Zuilen et al., 2002), which, if unrelated to measurement technique (Hayes, 1996), is consistent with such a prediction. On the other hand, isotopic measurements of reduced carbon from broadly correlative but less highly altered metasediments in the Isua region show only limited variation (Rosing, 1999). The same holds for organic carbon in 3.4–3.5 Ga rocks from the Onverwacht Group, South Africa, and the Warrawoona Group (Strauss & Moore, 1992). These data, sketchy as they are, provide our best current evidence for early autotrophy. Clearly, however, they place only limited constraints on the nature of Early Archean physiologies. More persuasive evidence for cyanobacteria comes from >C31 2α-methylhopanes (2Me-hopanes) recovered from 2.7 Ga bitumens in north-western Australia (Brocks et al., 1999). Summons et al. (1999) showed that that many cyanobacteria synthesize 2-methylbacteriohopanepolyol (2-MeBHP), the precursor compound to the 2Me-hopanes. Indeed, only cyanobacteria are known to produce this compound in concentrations likely to account for its abundance in Precambrian sedimentary rocks. Nonetheless, geological interpretation turns on the phylogenetic distribution of 2-MeBHP synthesis, which remains incompletely known. It appears that not all cyanobacteria produce 2-MeBHP (Summons et al., 1999). If this biosynthetic capability evolved only within derived lineages of cyanobacteria, we are in good shape – in this case oxygenic photosynthesis must have evolved before the ability to synthesize 2-MeBHP, and 2-Me-hopanes can be used as geological proxies for oxygenic photoautotrophs. If, however, 2-MeBHP occurred in the last common ancestor of all cyanobacteria, then we have no way of knowing whether coupled photosystems or 2-MeBHP arose first along the evolutionary pathway to modern cyanobacteria. Unless the two traits originated simultaneously, stem group cyanobacteria could have featured 2-MeBHP synthesis but not oxygenic photosynthesis, or vice versa, and should abundant 2-MeBHPs be found in heliobacteria or other clades, the interpretational difficulties will spiral. So, the antiquity of oxygenic photosynthesis is, in fact, difficult to establish. The presence of steranes in the same 2.7 Ga
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c. 2000 Ma cherts from the Belcher Islands, Canada (Golubic & Hofmann, 1976; Hofmann, 1976; Fig. 1B,C). Earlier entophysalids may occur in 2500 Ma cherts of the Transvaal Supergroup, South Africa, but poor preservation limits confidence in this interpretation (Altermann & Schopf, 1995). Older microfossils are not only rare and contentious, they do not have morphologies that are diagnostic for cyanobacteria. We must be particularly aware of this when we attempt to interpret putative microfossils in nearly 3.5 Ga rocks of the Warrawoona Group, Australia (Schopf & Packer, 1987; Schopf, 1992), and elsewhere (Walsh, 1992; Knoll & Barghoorn, 1977; Walsh & Lowe, 1999; Rasmussen, 2000). If biological at all (Brasier et al., 2002; Schopf et al., 2002), these do not possess features that can be used to constrain physiology. There is no compelling reason to interpret them as cyanobacterial. What about stromatolites, generally interpreted as the trace fossils of cyanobacterial mat communities? Paralleling the microfossil record, many Proterozoic stromatolites preserve petrological fabrics indicative of cyanobacterial participation in lamina accretion (e.g. Bertrand-Sarfati, 1976; Knoll & Semikhatov, 1998). Nearly all of these formed by the trapping and binding of fine-grained sediments by microbial communities. More problematic are stromatolites that accreted by the repeated precipitation of mineral laminae. We know that microbial mats can facilitate carbonate precipitation, but other processes can do so as well, making the biological interpretation of precipitated stromatolites difficult (Grotzinger & Rothman, 1996). For example, silicified Palaeo- and Mesoproterozoic carbonates show that the microdigitate stromatolites common in rocks of this age consist of stacked crystal fans whose relationship to microbiology in general and cyanobacteria in particular is difficult to establish (Hofmann & Jackson, 1987). The problem, as John Grotzinger first recognized, is that as we recede further back in time, the ratio of precipitated to trapped and bound stromatolites increases. In consequence, the proportion of stromatolitic structures that can be interpreted with confidence as products of cyanobacterial communities declines with age (Grotzinger & Knoll, 1999). Stromatolites occur in Early Archean successions, and, not surprisingly, their interpretation is controversial (Buick et al., 1981; Lowe, 1994). In some cases, especially the conical structures found in 3.45 Ga rocks of the Warrawoona Group (Hofmann et al., 1999), accretion may have been facilitated by micro-organisms, but the case for cyanobacterial involvement remains to be made. If fossils and stromatolites fail us, what about carbon isotopes? These provide some of our deepest historical insights into metabolism, and certainly the fractionation observed in reduced carbon as old as 3.8 Ga is consistent with CO2 fixation via the Calvin–Benson cycle (Rosing, 1999). But, as noted above, proteobacteria as well as cyanobacteria fix carbon this way. Moreover, it is difficult to rule out the possibility that Early Archean carbon was fixed via the reductive acetyl coenzyme A pathway, which fractionates C-isotopes by up to 34 – 40‰, or

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Fig. 2 Geological time-scale showing palaeontological and geochemical constraints on the antiquity of oxygenic photosynthesis (cyanobacteria), as well as the inferred redox history of the oceans and atmosphere. Phanero = Phanerozoic Era. See text for discussion and references.

shales that contain 2-Me-hopanes provides further, inferential support for the antiquity of oxygenic photosynthesis because the sterols from which these steranes were derived require molecular oxygen for their synthesis (Jahnke & Klein, 1983). The required partial pressures of oxygen are not high and could have been restricted to local oxygen oases (Knoll, 1999). Nonetheless, if we can rule out contamination by younger materials, the simultaneous presence in 2.7 Ga bitumens of steranes and 2-Me-hopanes suggests that cyanobacteria were present in Late Archean ecosystems (Fig. 2). Further supportive evidence for this conclusion comes from similarly ancient stromatolites with palimpsests of phototrophic microbes that occur in sulphate-deficient lakes formed on basalt basement (Buick, 1992). No metabolic reagents other than CO2 and H2O were available in these restricted evaporitic basins, so the only plausible method of primary production was oxygenic photosynthesis by cyanobacteria. Of course, cyanobacteria may have evolved much earlier. Nothing in the earlier record precludes an Early Archean origin of oxygenic photosynthesis – it is just that nothing we know at present requires such an early origin. The geobiological consequences of oxygenic photosynthesis When, then, did Earth’s atmosphere turn oxic? Debate about the Archean atmosphere continues, but most workers accept
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that the atmosphere generated by early outgassing was neutral to mildly reducing and that it did not become strongly or persistently oxidizing for some two billion years (for a dissenting view, see Ohmoto, 1996). Traditionally, arguments about oxidation history have relied on the temporal distributions of detrital uraninite, pyrite, siderite and banded iron formation (Cloud, 1968; Holland, 1984; Rasmussen & Buick, 1999). Uraninite, siderite and pyrite all oxidize readily in the presence of oxygen. Thus, their accumulation as detrital grains in well-aerated fluvial sediments deposited before c. 2.4–2.2 Ga and their rarity thereafter implies low oxygen concentrations in Archean and earliest Proterozoic air. Holland and colleagues (e.g. Rye & Holland, 1998) have added palaeosol chemistry to the mix, arguing that Fe released by chemical weathering will be lost when ground waters are anoxic, but retained quantitatively when ground waters carry oxygen. Weathering horizons developed before 2.4 Ga show substantial iron loss, whereas younger palaeosols retain weathered iron (Beukes et al., 2002). Still more recently, sulphur isotopes have been brought to bear on questions of Archean redox conditions. Cameron (1982, 1983) demonstrated two decades ago that S-isotopic fractionation in marine basins increased early in the Proterozoic Eon (Figs 2 and 3). Insofar as the environmental factor most likely to affect fractionation is sulphate availability (Habicht & Canfield, 1996), Canfield and colleagues

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Fig. 3 Diagram showing general patterns of secular variation in C and S isotopes through Archean and Proterozoic time, along with a broad estimate of atmospheric oxygen levels. ‘a’ denotes relatively high S-isotopic fractionation observed in evaporitic facies (but not open water deposits) of the 3.45 Ga Warrawoona Group (Shen et al., 2001). See text for discussion and references.

(Canfield & Teske, 1996; Canfield & Raiswell, 1999; Canfield et al., 2000) interpret this pattern in terms of a growing oceanic sulphate reservoir related to increasing oxygen in the atmosphere and surface ocean. Consistent with this view, an early Palaeoproterozoic decline in organic carbon characterized by unusual 13C depletion appears to record a global decline in the importance of methanogenesis in the recycling of marine organic matter (Hayes, 1994; Des Marais, 1997). Mass-independent S-isotopic fractionation also supports the idea of low pre-Proterozoic oxygen tensions. Farquhar et al. (2000) detected mass independent fractionation of sulphur isotopes in sedimentary sulphur species formed before c. 2.4 Ga but not after about 2.1 Ga. They propose that this pattern reflects the transition from a sulphur cycle governed by photochemical processes in an oxygen-free atmosphere to one dominated by oxidation during continental weathering and biological processes in the oceans. Thus, a case can be made that oxygen tensions increased globally at c. 2.4 Ga. This establishes a firm minimum date for the origin of cyanobacterial photosynthesis, but, as noted above, blue-greens likely existed at least 300 Ma earlier, and they may have evolved long before than that. Regardless of when oxygenic photosynthesis began, however, it cannot provide a sufficient explanation for Earth’s current atmospheric

inventory, because it appears that oxygen began to approach its modern state only much later in Earth history (Knoll et al., 1986; Derry et al., 1992; Knoll, 1992; Canfield & Teske, 1996; Shen et al., 2002a). Banded iron formations disappeared at c. 1700 Ma, requiring that substantial portions of the deep ocean remained anoxic well after 2400 Ma. And Canfield (1998) has proposed that, when it occurred, the cessation of iron deposition recorded not the oxidation of deep waters but rather the growth of a sulphate reservoir sufficient to drive sulphate reduction at rates capable of removing iron by reaction with H2S. According to Canfield, then, the mid-Proterozoic deep ocean was predominantly sulfidic, not oxic. Geochemical tests of this hypothesis are few, but growing. Shen et al. (2002) examined S-isotopes and Fe-speciation chemistry of c. 1730 Ma and 1640 Ma black shales deposited during maximum flooding events in the northern Australian Tawallah and McArthur groups, respectively. Iron chemistry suggests deposition beneath anoxic bottom waters, as occurs today in the Black Sea. Also, the limited fractionation and low variance displayed by S-isotopes in sedimentary pyrites from Tawallah and McArthur shales suggest (a) that much sulphate reduction occurred in the water column and (b) that sulphate was substantially depleted in these deep waters – requiring that well into the Proterozoic, sulphate reservoirs were much lower
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Geological consequences of evolution than today. Continuing research by Shen et al. (2003) shows that basinal black shales of the < 1500 Ma Roper Group also record anoxic deep waters and low sulphate abundances. Both deep water anoxia and low sulphate abundance can be local rather than global features of preserved basins. Australian data indicate that in this one corner of the world, however, low oxygen and low sulphate characterize preserved basinal successions through some 250 million years of mid-Proterozoic history. Independent studies by Lyons et al. (2000) in the Belt Supergroup and Kah et al. (2001) in younger Mesoproterozoic successions from Baffin Island also suggest that midProterozoic sulphate levels were low relative to today’s. Indeed, increasing data support the hypothesis that modern sulphate and oxygen levels may only have been approached near the end of the Proterozoic, just before the Ediacaran radiation (Hurtgen et al., 2002). Until late in the Proterozoic Eon, maximum S-isotopic fractionation rarely if ever exceeded the upper limit of 45‰ associated with bacterial sulphate reduction (Canfield & Teske, 1996; Fig. 3). The larger fractionations (up to 70‰) found in Phanerozoic sedimentary rocks originate when sulphur compounds formed by the oxidation of hydrogen sulphide undergo disproportionation to produce sulphate and sulphide. Canfield (1998) argued that we do not see these larger fractionations in older Proterozoic successions because hydrogen sulphide generated in anoxic deep waters was taken up by anoxic photoautotrophs before it came into contact with oxygenated surface waters – that in most Proterozoic oceans the redoxcline fell within the photic zone. By extension, the prominence of larger fractionation in successions deposited during the past 600 million years suggests that since this time, oceans have been more fully oxygenated. The abundance and distribution of oxygen in Proterozoic oceans remains contentious, as does the timing and mechanism of proposed Neoproterozoic increase in O2 levels (e.g. Anbar & Knoll, 2002). Nonetheless, it appears increasingly likely that although the innovation of oxygenic photosynthesis occurred once, early in our planet’s history, the oxidation of the oceans and atmosphere was a protracted affair that played out episodically over two billion years (Figs 2 and 3). Why is there this historical mismatch? Why didn’t the evolution of oxygenic photosynthesis rapidly engender an oxygenrich biosphere? In no small part, of course, it is because oxygenic photosynthesis forms a tight metabolic redox couple with aerobic respiration. Moreover, oxygen is also consumed by reaction with minerals and reduced volcanic gases (commonly mediated by micro-organisms). In geological time, then, oxygen fluxes to the atmosphere will reflect not gross photosynthesis, but the net balance between oxygen production and oxygen consumption by aerobic respiration and oxidation of inorganic materials. Because organic carbon burial effectively decouples photosynthesis and respiration, and because mid-oceanic ridges and volcanoes supply reduced gases to the Earth surface system, tectonics assumes a driving role in atmospheric history, as
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many have recognized (e.g. Godderis & Veizer, 2000). Exactly what processes modulated the historical accumulation of oxygen in the atmosphere and oceans remains a subject for debate; recent proposals (not mutually exclusive) include hydrogen escape after methane photolysis in the upper atmosphere (Catling et al., 2001), phosphate limitation of primary production in early oceans (Bjerrum & Canfield, 2002) and small changes in the oxygen fugacity of the mantle that resulted in less reduced gas fluxes from volcanoes (Holland, 2002). It is further unclear why PO seems to have remained 2 at least broadly stable over long intervals of time. This, I suspect, is where we should seek biological control mechanisms. In any event, the role of photosynthesis is clear. Oxygenic photosynthesis was absolutely necessary for the development and maintenance of Earth’s contemporary atmosphere. Yet, what evolution did in this case was define the dimensions of biological participation in the Earth system. It was the interaction of biological processes with tectonics that determined the state of the system through time.

OXYGEN AND THE CONTINUING EVOLUTION OF PHOTOSYNTHETIC ORGANISMS
What about my second question? Has the continuing oxidation of the Earth surface system influenced the ongoing evolution of photosynthetic physiology? Unambiguously, the answer is ‘yes’. Rubisco, the key enzyme responsible for CO2 fixation in oxygenic photoautotrophs, evolved early in Earth history when PCO2 was high and PO2 negligible. This would be of limited relevance were it not for the fact that Rubisco functions as an oxygenase as well as a carboxylase. That is, oxygen competes with CO2 for binding sites in the Rubisco molecule (Larcher, 1983). In consequence, as PO has increased through 2 time and PCO declined, the oxygenase capacity of Rubisco has 2 become more and more of a physiological burden, eroding the net photosynthetic capacity of cyanobacteria, algae and land plants (Larcher, 1983). Photosynthetic organisms have evolved several distinct responses to these changing environmental circumstances. First, photoautotrophs have evolved an elaborate biochemical pathway (involving, in photosynthetic eukaryotes, the mitochondria and peroxisomes, as well as chloroplasts) for salvaging the products of RuBP oxidation. Known as photorespiration, this pathway returns carbon to the Calvin–Benson cycle, albeit at some energetic cost (Larcher, 1983). Second, photosynthetic organisms have evolved several mechanisms to limit the in vivo oxygenase activity of Rubisco. Photosynthetic bacteria, algae and land plants show marked phylogenetic variation in the chemical affinity of Rubisco for CO2 and in the degree to which given oxygen tensions affect rates of CO2 fixation – later evolving groups fix carbon more effectively in the face of ambient oxygen (Raven, 1997).

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ANDREW H. KNOLL substrates for another, and further constraints arise from the interactive nature of biogeochemical cycles. Biological participation in the Earth system may be governed by photosynthesis, but photosynthesis itself is modulated by the availability of fixed nitrogen, phosphorus and trace nutrients (Sterner & Elser, 2002). This codependence of elemental cycles must help to buffer the environmental effects of metabolic innovation. Third, structural as well as physiological innovations in photosynthetic organisms may affect the Earth system, but are most likely to do so if they result in a departure from the C:N:P ratios common to most organisms. In geological time, such departures have been rare; perhaps the best example is wood, which contains C, but not N or P. As Berner (1998) and others have argued, the evolutionary emergence of woody plants, with its consequences for the increased penetration of substrates by roots and the new reservoir of metabolically recalcitrant organic particles in soil and sediments, coincides in time with an inferred late Palaeozoic decrease in PCO2 and may have been its proximal cause. At the same time, the oxygen generated by photosynthesis has affected the continuing evolution of photosynthetic organisms. On the road connecting evolution and environment, traffic flows in both directions.

Also, many photoautotrophs have carbon concentrating mechanisms that maintain locally high CO2/O2 within cells. Many algae pump bicarbonate across the cell membrane, converting it to CO2 within the cell (Kaplan & Reinhold, 1999; Ghoshal & Goyal, 2001). Vascular plant adaptations include C4 photosynthesis, in which CO2 is fixed into the four carbon compounds oxaloacetate or malate by PEPcarboxylase, transported to specialized cells surrounding vascular tissues, released enzymatically by decarboxylation, and, finally, refixed via Rubisco to enter the Calvin-Benson cycle (Larcher, 1983; Leegood, 2002). C4 photosynthesis, thus, ensures locally high CO2/O2 in cells where Rubisco is active; CAM plants such as cacti do much the same thing, but segregate the two pathways of CO2 fixation in time rather than in space (Larcher, 1983). Photorespiration and carbon-concentrating mechanisms, seemingly the constructs of some biological Rube Goldberg, find evolutionary interpretation as responses to biospheric oxygenation necessitated by the functional constraints of Rubisco.

AN ATTEMPT AT GENERALIZATION
The foregoing discussion prompts several summary thoughts, at least some of which may point toward general features of the relationship between evolutionary innovation and environmental change. First, innovations in metabolism define the dimensions of biological participation in the Earth system, but they seldom determine the state of the system by themselves. Rather, each metabolism interacts with other components of the system to determine its state. Second, the redox coupling of nearly all important metabolic pathways places an important constraint on the capacity of metabolic innovation to drive Earth system state change. The products of a given metabolism nearly always provide

EVOLUTIONARY PROCESS IN ENVIRONMENTAL HISTORY
Having explored, through one example, the relationship between evolutionary innovation and environmental change, we need to ask about another relationship, that between evolutionary process and environmental history. Two iconic representations of biology help us to think about an answer. The first is a powerful evolutionary metaphor originally developed by Sewall Wright (1932): the adaptive landscape (Fig. 4A). In Wright’s conception, each point on the landscape

Fig. 4 Two iconic representations of biology: (A) the adaptive landscape, as illustrated by Wright (1932); (B) Daisyworld simulation of planetary temperature regulation by daisies with differing albedos, as depicted by Lovelock (1989). See text for discussion.

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Geological consequences of evolution surface represents a specific genotype; elevations reflect the relative fitness of different genotypes in a specified environment. Because of natural selection, new colonists placed in the landscape will tend to climb the nearest adaptive peak (not necessarily the highest one), quickly, in evolutionary terms, gaining its summit. Once a peak is occupied, the likelihood that further mutation will result in improved fitness declines to zero. In consequence, subsequent selection is largely stabilizing, acting to maintain the successful population – see, for example, Lenski & Travasiano’s (1994) experimental studies of adaptation in E. coli. While the environment remains steady, stasis – including the now classical palaeontological stasis of Gould & Eldredge (1993) – will be favoured. (Radical mutations may allow populations to jump from one adaptive peak to another, but the chances of that happening in an ecologically full world are small.) What happens, then, when a genotype contributes to change in its surrounding environment? In an altered fitness landscape, the genotype is likely to fall on an adaptive slope or valley rather than a peak. That is, changing the ambient environment has an evolutionary effect not dissimilar to deleterious mutation, decreasing the fitness of genotypes that formerly occupied adaptive peaks. It might seem therefore that selection should act to sustain genotypes best able to maintain local environmental stasis. There is, however, a wrinkle to this argument. While an altered adaptive landscape will probably decrease the fitness of genotypes that were maximally fit before, it may increase the fitness of other genotypes present in the population. That is, environmental change engendered by one genotype (or population or species) may well benefit a second genotype. This, of course, is just what happens among species during ecological succession (e.g. Lenton, 1998). Lansing et al. (1998) termed this response ‘system-dependent’ selection and argued that it will increase environmental regulation by the biota. I suspect that in the presence of biological variation, population genetics will commonly act as a buffer against biologically induced environmental change, but the buffer is weak and I have no confidence it will hold on evolutionary time-scales. This prompts consideration of a second icon, the Daisyworld model of biological control in the Earth system (Fig. 4B). In early formulations (e.g. Watson & Lovelock, 1983), Daisyworld is seeded in proximity to a sun whose luminosity increases through time. Initially, the temperature of Daisyworld is less than 5 °C, the minimum temperature for daisy growth. As solar luminosity, and, hence, surface temperature, increase, daisies begin to germinate, influencing the ambient environment as they grow by altering the planet’s albedo. All daisies grow best at 22.5 °C, but dark and light individuals differ in their capacity to absorb sunlight. In consequence, dark daisies are initially at an advantage and spread to cover the planet, warming it as they go. As solar luminosity increases, however, light daisies will begin to expand, and the changing mixture of dark and white individuals will act to
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maintain the planetary surface close to the optimal temperature for daisy growth as solar luminosity increases. The experiment ends when solar luminosity exceeds the buffering capacity of daisies, as dictated by their maximum growth temperature of 40 °C. Daisyworld owes its regulatory power to the fact that it specifies a fixed set-point, the optimum temperature for daisy growth (Weber, 2001). In its original, explicitly ecological form, this assumption seems reasonable, but what happens when we allow daisies to mutate and adapt? Robertson & Robinson (1998) modelled a Daisyworld in which evolving daisies shifted their optimal growth temperature to match their local environment. In consequence, the bioregulation observed in purely ecological models broke down (see also Lansing et al., 1998). Such simulations suggest that, by itself, system-dependent selection will not predictably endow ecosystems with negative feedbacks. Other homeostatic mechanisms must be afoot. Nonetheless, the parable of Daisyworld suggests two sensible conclusions. First, when applied at the right scale – required by both population genetics and physical interactions to be local not global (Weber, 2001; see Daly & Smith, 1993, for a real world example) – Daisyworld suggests that biological variation helps to buffer externally imposed environmental change. Second, the buffering capacity is limited. When extrinsic environmental forcing exceeds a certain threshold, homeostasis fails and the system moves to a new state. Ice ages illustrate the point. How, then, does the Earth system remain within a relatively narrow range of variation for long time intervals? The biological processes that contribute most effectively to environmental homeostasis are probably those mentioned earlier as constraints on the environment impact of evolutionary innovations: the linkage of complementary metabolisms in biogeochemical cycles and systems (Tateno & Chapin, 1997; Downing & Zvirinsky, 1999). If photoautotrophs deplete ambient CO2, biology’s most potent response is to decrease rates of photosynthesis while increasing respiration to restore carbon dioxide. Rates of growth and metabolism provide more sensitive controls on environmental homeostasis than population genetics. Of course, population genetic processes produce evolutionary innovations, and, as exemplified by the origin of wood, these may facilitate environmental state change. The geological record, however, suggests that more commonly the vector of causation has pointed in the other direction – that the alteration of fitness landscapes by imposed environmental change has facilitated evolutionary innovation. (I do not mean to imply that evolution occurs only in response to changes in the physical environment. Evolutionary change commonly reflects changes in the biological components of a species’ effective environment.) With change in the physical environment, dominant genotypes and populations have disappeared, and survivors and new colonists climbed emerging adaptive peaks. This is what happened when oxygen invaded the atmosphere.

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It is what happened when decreasing CO2 and increasing O2 forced new molecular complexities on photosynthetic physiology. It is what happens locally when sea level recedes and globally when a bolide collides with Earth.

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CONCLUSIONS
I cannot pretend that the foregoing thoughts provide satisfactory answers to any of the questions I have raised – geobiology remains in the opening lap of a very long race. I hope, rather, that my comments have illuminated a path by which answers will be discovered. Geobiologists must root their research in comparative biology, especially the physiological reactions that underpin metabolism. We must understand how biological and physical processes interact in the Earth system and, if we are to explore geobiology in Earth history (surely a grand theme of the Earth sciences), link systems ecology and population genetics more successfully than we have to date. Geobiology requires palaeontology, but a palaeontology focused more on metabolism than morphology (Knoll & Hayes, 2001) and the discoveries of palaeontologists must be interwoven with those of geochemists to form coherent histories that will inspire new efforts to model the dynamic Earth system. Earth is a biological planet, but not a planet formed (pace Lincoln) by the biota of the biota and for the biota. Rather we live on a planet that was habitable when life first emerged and which has remained habitable through the complex and incompletely understood interactions of biological and other components of the Earth system. That is not quite the world that James Hutton envisaged. In our modern worldview, biology is no more static than the land and sea in Hutton’s conception. But it is certainly in the spirit of his Theory of the Earth. This being the case, let me close by granting Hutton (1785) the final word: Thus, in supposing Nature to be wise and good, an argument is formed in confirmation of the theory, or, in supposing the theory to be just, an argument may be established for wisdom and benevolence to be perceived in nature. In this manner, there is opened to our view a subject interesting to man who thinks; a subject on which to reason with relation to the system of nature; and one which may afford the human mind both information and entertainment.

ACKNOWLEDGMENTS
This essay began life as an invited plenary lecture at the GSAGSL meeting on Earth System Processes, held in Edinburgh, Scotland, in June 2001. I thank Ian Fairchild, Ian Dalziel and the other organizers for issuing the challenge to think in this direction and Roger Buick, Jochen Brocks and an anonymous reviewer for helpful comments on the manuscript. Research leading to this paper was supported in part by the NASA Astrobiology Institute.

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