Perspective

The energy expansions of evolution

  • Nature Ecology & Evolution 1, Article number: 0138 (2017)
  • doi:10.1038/s41559-017-0138
  • Download Citation
Received:
Accepted:
Published online:

Abstract

The history of the life–Earth system can be divided into five ‘energetic’ epochs, each featuring the evolution of life forms that can exploit a new source of energy. These sources are: geochemical energy, sunlight, oxygen, flesh and fire. The first two were present at the start, but oxygen, flesh and fire are all consequences of evolutionary events. Since no category of energy source has disappeared, this has, over time, resulted in an expanding realm of the sources of energy available to living organisms and a concomitant increase in the diversity and complexity of ecosystems. These energy expansions have also mediated the transformation of key aspects of the planetary environment, which have in turn mediated the future course of evolutionary change. Using energy as a lens thus illuminates patterns in the entwined histories of life and Earth, and may also provide a framework for considering the potential trajectories of life–planet systems elsewhere. Correspondence (14 August 2017)

Free energy is a universal requirement for life. It drives mechanical motion and chemical reactions—which in biology can change a cell or an organism1,2. Over the course of Earth history, the harnessing of free energy by organisms has had a dramatic impact on the planetary environmen3,​4,​5,​6,​7. Yet the variety of free-energy sources available to living organisms has expanded over time. These expansions are consequences of events in the evolution of life, and they have mediated the transformation of the planet from an anoxic world that could support only microbial life, to one that boasts the rich geology and diversity of life present today. Here, I review these energy expansions, discuss how they map onto the biological and geological development of Earth, and consider what this could mean for the trajectories of life–planet systems elsewhere.

In the beginning

From the time Earth formed, around 4.56 billion years ago (Ga), two sources of energy were potentially available to living organisms: geochemical energy and sunlight. Sunlight is a consequence of the planet's position in the Solar System, whereas geochemical energy is an intrinsic property of the Earth. Geochemical energy arises when water reacts with basalts and other rocks8,​9,​10. These water–rock reactions—which continue today11—generate reduced compounds such as hydrogen, hydrogen sulfide, and methane8,​9,​10. Oxidation of these compounds releases energy, which organisms can capture and store in the form of chemical bonds. Although sources of geochemical energy can be at or near Earth's surface, they need not be: many are deep within the planet, out of reach of sunlight.

Assuming that life did not parachute in, fully formed, from elsewhere, a number of authors12,​13,​14,​15 have argued that the transition from non-life to life took place in the context of geochemical energy, with the ability to harness sunlight evolving later (Fig. 1). Consistent with this, both phylogenetic16 and biochemical13,17 evidence suggest that the earliest life forms were chemoautotrophs, perhaps living by reacting hydrogen with carbon dioxide and giving off acetate, methane and water13,16. Mounting evidence18,​19,​20,​21,​22 suggests that the transition from non-life to life may have taken place before 3.7 Ga—a time from which few rocks remain23.

Figure 1: Key events during the energy expansions of evolution.
Figure 1

(i) Life emerges; epoch of geochemistry begins. (ii) Anoxygenic photosynthesis: start of energy epoch 2, sunlight. (iii) Emergence of cyanobacteria. (iv) Great Oxidation Event: energy epoch 3, oxygen. (v) Probable eukaryotic fossils appear. (vi) Fossils of red algae appear. (vii) Start of energy epoch 4, flesh. (viii) Vascular plants colonize land; fire appears on Earth. Finally, the burning logs indicate the start of energy epoch 5, fire. The dates of (i)–(iii) are highly uncertain. For (i) I have taken the earliest date for which there is evidence consistent with life20. For (ii) I have taken the earliest date for which there is evidence consistent with photosynthesis18,19,21. For (iii), I have marked the date currently supported by fossil evidence for the presence of cyanobacteria (see main text, ‘Cyanobacteria and the oxygenation of the air’). Tick marks represent intervals of 25 million years. Figure drawn by F. Zsolnai.

Energy epoch one: geochemical energy

Analysis of biochemical pathways suggests that, under favourable environmental conditions, early autotrophs could readily have adopted a heterotrophic lifestyle, feeding on the contents of dead cells24. At this time in Earth history, oxygen was at trace levels25, so the first ecosystems would have been anaerobic.

Early ecosystems may have quickly diversified to take the form of a microbial mat, where the waste products of one group of life forms feed the metabolism of another26,27. Such an arrangement generates layered communities of organisms, each layer having a different metabolic speciality28,29. In anaerobic ecosystems of this type, mobile predation is essentially nonexistent: growth rates are so low that hunting and consuming other organisms doesn't yield enough energy30. Viruses, however, are likely to have been an important force from early in the history of life31. They act as agents of death—and by lysing cells, they would have provided additional sources of organic carbon to heterotrophs. Viruses also transport genes from one host to another, and thus may have enabled the spread of evolutionary innovations. Many of the coevolutionary selection pressures of the modern biosphere would have been minimal (for example, predation and the opportunity to live inside other organisms) or absent (for example, sexual selection).

The niches available would have been those near sources of geochemical energy, suggesting a patchy, local distribution of life. Consistent with this, geochemical models32,​33,​34 suggest that the productivity of the biosphere before it was powered by the sun would have been at least a thousand times less than it is today, and may have been one million times less.

Owing to the scarcity of rocks from Earth's remote past, the impact of early life on the planetary environment is also hard to assess. Life inevitably creates a suite of changes in its environment (Box 1), and the establishment of life would have initiated biogeochemical cycling, but owing to the low productivity of the biosphere, the initial effects are likely to have been small32,​33,​34.

Box 1: Transforming life.

The capacity of life to transform a planetary environment arises from the fact that life automatically generates several epiphenomena. These are: metabolism, evolution, acceleration and redistribution.

Metabolism causes transformations of inanimate matter, as when a methanogen transforms hydrogen and carbon dioxide into methane and water. Metabolism thus mediates the ‘bio’ part of biogeochemical cycles. Evolution expands metabolic variety, increases the efficiency with which life consumes energy and resources, and over time, expands the breadth of life's grip on the cycling of the elements.

Acceleration arises from the fact that enzymes catalyse reactions that would otherwise happen slowly, if at all. Sometimes the acceleration is extreme, achieving in 18 milliseconds a reaction that would otherwise be expected to take 78 million years, an improvement of 20 orders of magnitude154. Many life-mediated accelerations also include huge improvements in the temperatures and pressures at which reactions can occur. For example: the smectite-to-illite reaction, a transformation between two clay minerals. In the absence of microbial involvement, this transformation requires 4–5 months at 300 °C and high pressure (1,000 atmospheres). In the presence of the bacterium Shewanella oneidensis, the same reaction takes just two weeks—at room temperature and one atmosphere155.

Finally, living organisms redistribute and restructure the physical fabric of the planet. For much of Earth history, the effect was one of concentration. For example, living organisms tend to concentrate the lighter isotopes of elements such as carbon or sulfur inside their bodies156,157; they can also produce large accumulations of materials such as limestone. But with the advent of energy epoch 4 (see main text, ‘Energy epoch four: flesh’), living organisms also began large-scale mixing of sediments and the transport of materials from the land to the sea, and from the sea surface to the deep sea and back again.

These epiphenomena will occur wherever life does. However, the magnitude of their impact will depend on life becoming abundant. If life is limited (whether by the availability of energy, resources, or evolutionary developments), the potential for life to transform a planet will be small.

Energy epoch two: sunlight

At some point early in the history of the Earth—perhaps by 3.7 Ga18,19,21 (Fig. 1)—organisms evolved to harness the energy in sunlight to drive chemical reactions. Today, several groups of bacteria engage in photosynthesis, using a variety of different pathways35. One pathway, oxygenic photosynthesis, gives off oxygen as a by-product; the others, all forms of anoxygenic photosynthesis, do not. Genetic35, fossil36, and biochemical37 evidence all suggest that of the two, anoxygenic photosynthesis evolved first.

Because sunlight is abundant across the planet's surface, the ability to use it made far more of the planet available to life. Consistent with this, models of the early Earth suggest that the advent of anoxygenic photosynthesis greatly increased the productivity of early ecosystems32,33. At the same time, microbial ecosystems were able to become more diverse. Forms of photoheterotrophy38 may also have begun to evolve. This lifestyle does not involve fixing carbon—organisms still require a source of organic carbon—but does involve transducing sunshine into ATP, which reduces energy needs from other sources.

During this epoch, the impact of life on the planetary environment expanded too. Structures such as stromatolites39 and banded iron formations19 began to appear, and methane may have started to build up in the atmosphere40. Indeed, the climate of the early Earth appears to have been temperate41 despite the fact that, back then, the sun had only about 70% of its current brightness42. Methane, along with ethane, which can be produced from methane by photochemical reactions in the atmosphere43, are greenhouse gases: thus, methane production on the part of living organisms may have helped to keep the early Earth from freezing25,43.

But the crucial event of this period—the one that would go on to have by far the most biological and geological impact—was the evolution of oxygenic photosynthesis, an innovation that appeared in just one phylum, the cyanobacteria.

Cyanobacteria and the oxygenation of the air. In the absence of a biotic source of oxygen, trace quantities of the gas can be generated abiotically: water molecules can be split by sunlight44 or radioactive decay45. However, these abiotic processes are much less efficient than their biotic equivalent34,44. Had cyanobacteria, or something like them, never evolved, oxygen would never have built up in the atmosphere of the Earth.

But build up it did. Between 2.45 and 2.32 Ga (ref. 46), significant quantities of oxygen began to accumulate in the air, an episode known as the Great Oxidation Event. Before the Great Oxidation, atmospheric oxygen levels were less than 10−5 of the present atmospheric level of 21%. By 2 Ga, they had risen to perhaps 0.1–1% of the present atmospheric level25. Although the subsequent history of oxygen is complex and many details are uncertain47,48, Earth's atmosphere has contained an appreciable level of the gas ever since. (Full oxygenation of the oceans, however, would not happen until around 1.8 billion years after the Great Oxidation47.)

Of all the events in the early history of the Earth, the Great Oxidation is the least controversial. It marks a line across the history of the planet, with a suite of geological markers showing a shift in the prevailing chemistry44,49. In contrast, there is enormous uncertainty about when cyanobacteria first evolved, with estimates spanning a period of one billion years35,47. However, genetic50, fossil51, and geochemical47,52 evidence all suggest that cyanobacteria evolved at least 300 million years before the Great Oxidation Event.

But if cyanobacteria evolved hundreds of millions of years before the Great Oxidation, why did oxygen take so long to accumulate? This question has been studied extensively, and various hypotheses have been put forward (for a review see refs 25,53). In essence, though, it's a matter of planetary chemistry. Both the atmosphere and ocean of the early Earth were full of molecules such as hydrogen, methane and ferrous iron that oxygen reacts with; oxygen may thus have been removed as fast as it was produced25,54. Until sources of oxygen began to exceed the sinks, the gas would have been unable to accumulate25.

Even before the Great Oxidation, the emergence of cyanobacteria would have increased both the productivity and complexity of microbial ecosystems. As well as a variety of heterotrophs, modern microbial mats and stromatolites often contain photosynthetic organisms of several different types55. Moreover, in evolving to extract electrons from the hydrogen in water, rather than from substances such as ferrous iron or hydrogen sulfide, cyanobacteria would have been far less constrained in the habitats they could occupy. Cyanobacteria may even have been among the first organisms to colonize land surfaces56, increasing the weathering of rocks, and thus the flow of nutrients into the oceans57. But these impacts are dwarfed by those that resulted from the accumulation of oxygen in the air.

Oxygen and the planetary environment. The Great Oxidation Event had a dramatic impact on the planetary environment. First, the transition to an oxygen-rich atmosphere took place in tandem with the establishment of the ozone layer54,58,59, thus changing the physical context in which organisms, especially those on land, evolve. Second, the diversity of minerals at the Earth's surface began to increase60, eventually more than doubling61.

Third, the appearance of atmospheric oxygen created a variety of new abiotic niches. As well as the anoxic and micro-oxic niches that had existed from the outset, the oxygenation of the atmosphere created an abundance of oxygen-rich niches, too. Today, aerobic prokaryotes show an enhanced ability to tolerate extremes of salinity and pH compared to their anaerobic counterparts62, suggesting that the availability of oxygen might also have allowed for the colonization of other, previously inaccessible, abiotic niches. At the same time, the availability of oxygen would have increased the availabilities of oxidants such as nitrate and sulfate—and thus would also have increased the productivity of chemotrophic life forms.

Fourth, the Great Oxidation seems to have coincided with a series of extreme ice ages63. The reasons for this are unresolved63, but some authors25,64,65 have suggested it could have been due to a decline in the flux of biogenic methane reaching the atmosphere, and a corresponding decline in the contribution of methane and its byproducts to keeping the climate warm.

But the most significant environmental impact of the Great Oxidation was a change in the prevailing chemistry, and the ready availability of oxygen gas as a source of energy for living organisms.

Energy epoch three: oxygen

Oxygen is a rich source of energy: the use of oxygen as an electron acceptor releases more energy per electron transfer than that of any other element except for chlorine and fluorine66. (Neither chlorine nor fluorine is cosmically abundant, however, and both are so reactive as to be an unlikely foundation for any kind of biology66.) The diversification of the biosphere that would ultimately take place was, to a large extent, enabled by the growing abundance of oxygen.

The emergence of the ability of living organisms to use oxygen as an energy source is shrouded in at least as much mystery as the emergence of cyanobacteria. At issue is whether early life forms could have evolved to use trace oxygen or hydrogen peroxide produced through abiotic processes67—and thus whether aerobic respiration originated before the advent of cyanobacteria, or whether it evolved in conjunction with them. Whatever the case, long before the Great Oxidation Event, aerobic organisms, if they existed, could have prospered in oxygen-rich oases generated by cyanobacteria68,69.

As well as being a source of energy, oxygen is both a biological problem and an opportunity. Problem: the presence of oxygen inactivates some enzymes, and oxygen derivatives such as hydrogen peroxide and the superoxide ion are reactive compounds that damage both DNA and proteins70,71. To survive in the presence of oxygen, organisms need a superstructure of protective enzymes. Opportunity: the availability of oxygen permits the construction of new molecules, such as collagen72.

During this epoch, two momentous events took place: the emergence of eukaryotes and the emergence of the lineage that would eventually produce land plants. Both events represent fusions between two previously independent lineages, an archaeon and an alphaproteobacterium in the case of eukaryotes73,74, and a eukaryote and a cyanobacterium in the case of the plant lineage75; the alphaproteobacterium evolved to become the mitochondrion, the cyanobacterium, the chloroplast. Both events thus also represent important shifts in the capacity for organisms to transduce energy. Fossils of red algae show that both events had taken place by 1.2 Ga (ref. 76), and microfossils that are probably eukaryotic in origin date to 1.8 Ga (ref. 77).

In extant eukaryotes, organelles of mitochondrial origin take several different, but related, forms78. Notably, only one—the ‘standard’ mitochondrion found, for example, in humans—requires oxygen. Three others are involved in forms of anaerobic metabolism; of these, two produce hydrogen. These observations fit with the hypothesis, advanced by Martin and colleagues74,79, that the ancestral eukaryote resulted from a prior symbiotic association between a hydrogen-dependent archaeon and a metabolically flexible alphaproteobacterium that, in the absence of oxygen, lived anaerobically producing hydrogen, and in the presence of oxygen, lived aerobically. If this hypothesis is correct, the ancestral eukaryote could have been a facultative anaerobe, able to live in both oxic and anoxic environments. Such a scenario not only accounts for the different types of mitochondria seen in extant eukaryotes78, but also for the fact that, today, species with mitochondria that produce ATP through anaerobic pathways are sprinkled across the eukaryotic tree while exhibiting a similar underlying biochemistry78,80.

Eukaryotes differ from prokaryotes in many respects, from meiosis and syngamy to the presence of a cell nucleus, as well as a suite of other features. In addition, complex multicellularity and large size has evolved only in eukaryotes—which Lane and Martin81 have attributed to an enhanced capacity to generate energy owing to the possession of mitochondria (Box 2). From the point of view of the biosphere, the emergence and diversification of eukaryotes provided a new set of niches for prokaryotes to occupy—which in turn allowed eukaryotes to occupy a far wider variety of niches. Today, most, perhaps all, eukaryotes have symbiotic dependencies on consortia of prokaryotes—microbiomes—that give them access to a greater variety of energy sources and metabolic capabilities82.

Box 2: Life and energy.

Living organisms gather energy from external sources and transduce it into ATP molecules. By breaking the bonds in ATP, they can use energy in the cell to do work such as copying DNA, building proteins, maintaining their cellular structures, growing, powering their flagellae, and so on. Of these activities, building proteins is particularly expensive, accounting for a significant proportion of a cell's total energetic costs.

Lane and Martin81 argue that the fundamental difference between prokaryotes and eukaryotes is one of energy limitation. They suggest that, owing to the mechanics of ATP synthesis, prokaryotes are intrinsically limited in the amount of ATP they can manufacture—and thus, in the number of proteins they have the power to build.

Eukaryotes, they argue, are not limited in this way because their cells contain large numbers of mitochondria—the sites of ATP synthesis. Mitochondria are the descendants of the alphaproteobacterium that, long ago, fused with an archaeon to form the ur-eukaryotic cell. Today, mitochondrial genomes are highly reduced compared with that of their bacterial ancestor, but the genes they have kept are those important for the local regulation of ATP production158. With so much more ATP available at so little extra expense, the evolution of mitochondria released the ancestral eukaryote from an energetic constraint, allowing for the episode of proteome expansion159 that coincides with the emergence of the eukaryotic cell. This difference in energetic potential, Lane and Martin suggest, is the reason that prokaryotes have remained small and morphologically simple, while eukaryotes have been able to radiate through a landscape of complex shapes and extreme bigness.

More generally, the need to use energy efficiently can mould the finest details of living organisms. For example, life forms often evolve to reduce the costs of building particular proteins160,​161,​162. The reason is that amino acids vary in how much energy they take to make163. Especially when a protein is made in large quantities, such differences add up. Thus, over time, mutations that cause ‘expensive’ amino acids to be replaced by ‘cheaper’ ones tend to be favoured—so long as the replacement does not interfere with the protein being able to function.

For the purposes of this Perspective, however, one feature of eukaryotes is particularly important. This is the ability to engage in phagocytosis—the engulfment of particles and, sometimes, other life forms. The wholesale engulfment of other beings appears to be a eukaryotic invention83, and it whets the appetite for:

Energy epoch four: flesh

Around 575 million years ago (Ma), during the Ediacaran Period, a new form of life began to become abundant: animals84. And with animals would soon come a powerful new force of nature: the acquisition of energy through the active hunting and eating of other life forms, especially, other animals. This would produce a radical shift that, within a mere 40 million years, transformed the Earth. Before this epoch, ecosystems were microbial. The advent of widespread flesh-eating launched the Phanerozoic, triggering an enormous increase in organism size85, a new tempo of macroevolutionary change86,87, new kinds of ecosystems86,​87,​88, and an increased impact of life on the fabric of the planet87.

As in the case of oxygen, however, flesh-eating has a prehistory. Predation by single-celled eukaryotes may have caused the evolution of the first armoured algae, around 770 Ma89,​90,​91, as well as a major increase in eukaryotic diversity92. Moreover, animals represent one of several transitions to complex multicellular life93—transitions that Stanley86 suggested might, in part, have resulted from single-celled eukaryotes engulfing and consuming each other. Indeed, molecular clocks show that the first animals also evolved around this time94,95 (Box 3), leading Knoll and Lahr92 to propose that tiny animals might have helped drive the diversification of eukaryotic protists.

Box 3: Oxygen and the evolution of animals.

No one disputes that ample oxygen is a prerequisite for the evolution of large, mobile animals—that no other substrate provides enough energy to power them. But a major point of contention concerns the role of oxygen in the early evolution of animals164. The question has two parts: how much oxygen was required for their initial evolution, and how much for their spectacular and rapid diversification, more than 200 million years later, at the start of the Cambrian?

The answer to the first part is: not much165. Like the earliest eukaryotes, the earliest animals may well have had mitochondria that were faculatively anaerobic78,165, and thus would have been able to persist in environments where oxygen levels were low or unstable.

However, low oxygen limits animal ecology in several ways. Without a good supply of oxygen, animals cannot grow big or move fast: they cannot get enough power. A neat demonstration of this comes from work by Sperling and colleagues166. Using data from modern oceans, these authors showed that in low oxygen regions, there can be plenty of animals, but they tend to be small and passive. Active predators—flesh eaters—only appear once oxygen levels become more moderate. Another point to note is that without access to oxygen, animals cannot make collagen, one of their main connective tissues. Without collagen, they cannot leave body fossils72.

Such observations have led a number of authors167,​168,​169,​170 to wonder whether a rise in oxygen permitted the Cambrian Explosion by releasing an important evolutionary constraint. Although evidence for a rise in atmospheric oxygen towards the end of the Proterozoic is mixed (and disputed), it seems that parts of the deep ocean became well oxygenated around this time, leading Lenton and colleagues171 to suggest that—even in the absence of a rise in atmospheric oxygen—the activities of the earliest animals could have facilitated the oxygenation of the oceans, which in turn could have facilitated the evolution of larger, faster, hungrier animals.

Today, animals influence diversity at all levels of an ecosystem, with grazers such as slugs96 or zooplankton97 maintaining the diversity of plants or phytoplankton, and carnivores such as wolves98 maintaining the diversity of plants through their predation on herbivores. This kind of ecology—complex food webs with many types of eaters—was absent from Earth until around 550 Ma, when the first animals that eat animals evolved. Their appearance seems to have triggered the rapid diversification of animal life sometimes referred to as the Cambrian Explosion.

In addition to their effects on the structure of ecosystems, the flourishing of flesh-eating animals heralded a step-change in both biomass and biodiversity87. In the oceans today, for example, Butterfield87 has estimated that animals may comprise as much as 80% of the biomass in the pelagic zone. Furthermore, with the evolution of animals, new coevolutionary selection pressures—in particular, arms races between the eaters and the eaten—appeared, accelerating the pace of macroevolution99. At the same time, animal guts and external surfaces provided new niches for other life forms, both symbiotic and hostile.

On the geological side, the flourishing of animals had at least four major impacts. First, the evolution of predation rapidly led to the evolution of armour—shells, scales, spikes and carapaces built from materials such as calcite and silica100. Although, as noted above, the first protective coverings (on algae) date back to around 770 Ma (ref. 90), it's not until the evolution of flesh-eating animals that shells and other forms of protection became widespread. This development would eventually result in vast deposits of materials such as radiolarite101, limestone102, coquina103 and chalk104 and would also produce changes in ocean chemistry, as organisms removed dissolved materials such as silica and calcium and used it for themselves105,106.

Second, animals produce faeces, which have important effects on the way that nutrients are distributed around the globe. For example, in the ocean, zooplankton faecal pellets sink more rapidly than individual algal or bacterial cells, and thus transport organic matter from the surface to the seabed107. Today, the faeces of sperm whales bring iron from the deep sea to the ocean surface108; the faeces of birds like cormorants transport nutrients from the ocean onto land, sometimes in fantastic quantities109.

A third geological impact of animals is caused by their ability to burrow. Simple, horizontal burrows appear in the fossil record around 555 Ma (ref. 110); by the early Cambrian, the abundance, size, depth and complexity of burrows had increased considerably110. Widespread burrowing creates a mixing of sediments known as bioturbation. As Darwin111 observed with respect to earthworms, burrowing is analogous to ploughing: it redistributes nutrients as well as sifting, irrigating, and aerating sediments and soils.

Finally, from bioturbation, faeces, and the evolution of armour, a fourth major impact of flesh-eating life forms emerges: a reorganization of Earth's biogeochemical cycles105,112,​113,​114.

Energy epoch five: fire

Of all the planets and moons in the Solar System, Earth is the only one to have fire. This is because, to have fire, all of three conditions must be met. (1) Fire needs a source of ignition—such as lightning strikes. Throughout Earth history, these have been abundant; today, there are more than 1.4 billion lightning strikes per year (ref. 115), of which an appreciable number ignite wildfires116. Lightning occurs on other planets117, but none of these meets the other two conditions. (2) Fire needs oxygen. Assuming current atmospheric pressure, Earth's air must contain at least 16% of the gas118,119. For most of Earth's history, oxygen levels have been lower than this threshold. (3) Fire needs fuel. So it is not until the evolution of vascular plants on land, around 420 Ma, that all three conditions were met120.

From the start, fire has had both geological and biological impacts. Fire regimes drive the evolution of plant traits121; fires affect soils and air quality; and although, each year, a significant amount of biomass goes up in smoke, fire can promote biodiversity122. Fire may even have driven the initial spread of flowering plants123—an event that led to radiations of many other groups, including ants124, bees125 and mammals126. Furthermore, fire contributes new material to the Earth—charcoal, ash and soot—and may also act as a control on planetary oxygen levels127. But as an energy source, per se? That's a more recent development, and has come in two phases.

The first phase began with the evolution of a fire creature. This creature—a member of the genus Homo128—began to control the use of fire, deliberately setting fires alight and using fire for cooking. Exactly when cooking began remains controversial, with possible dates ranging from 1.5 Ma to 0.4 Ma (ref. 129). The important point, though, is that cooking is a kind of predigestion: cooked food, be it meat130, vegetable130 or lipid131, delivers more energy than the same food eaten raw. In using fire to cook food, hominins thus developed a way to extract more energy from their diets, and to eat a wider variety of food.

The second phase of fire as an energy source is even more recent—but the onset is nonetheless difficult to pinpoint. Does it start with the use of fire to manufacture labour-saving tools? With the smelting of iron, something otherwise energetically impossible? With the burning of fossil fuels such as coal to generate heat and light? With the invention of the internal combustion engine? Or with the discovery of the Haber–Bosch process for fixing nitrogen—which, in 1925, Alfred Lotka132 described as the start of “a new cosmic epoch”? Perhaps these last three are the most important contenders, as together, they have transformed the planet7. In particular, the human input of energy to manufacture and deliver an otherwise limiting nutrient has produced far higher crop yields, enormously larger human populations, and gigantic populations of human-associated animals such as pigs, cows, horses and chickens133. Erisman and colleagues134 estimate that between 1908 and 2008, industrially produced nitrogen fertilizer supported an additional four billion people and that by 2008, nitrogen fertilizers were responsible for feeding 48% of the human population. Meanwhile, Pimm and colleagues135 judge that extinction rates are now 1,000 times greater than the typical background rate. In sum, in this epoch of fire, total biomass has remained high, but biodiversity has begun to fall.

The geological impacts of the age of fire are also poised to be dramatic, with rising levels of carbon dioxide and other greenhouse gases in the air, rising sea levels, increasing levels of nitrogen and plastic pollution, a remaking of the landscape with mines, tunnels, dams and cities, the introduction of new chemical compounds, and massive shifts in several biogeochemical cycles. However, the full geological effects of this epoch are, as yet, unknown.

Implications

Different schemata for considering the history of life allow different types of insights. For example, de Duve136 identified a series of (mostly) biochemical events that happened just once, and discussed to what extent they would be likely to happen again were the tape of life to be replayed. Knoll and Bambach137 put forward six ‘megatrajectories’ in the history of life, where each megatrajectory corresponds to the ecological diversification of a new type of life form (prokaryotes, unicellular eukaryotes, land plants, etc), thus linking evolutionary change with ecological complexity. And famously, Maynard Smith and Szathmáry138,139 proposed a framework based on transitions between different replicating units (genes, chromosomes, individuals, and so on); this has been profoundly helpful in generating a deeper understanding of the levels at which natural selection operates140.

In recent work, Lenton and colleagues7 developed a schema for thinking about ‘revolutions’ in the history of life and Earth. As in the Perspective presented here, their focus is energy. But rather than considering expansions in the types of energy underpinning the biosphere, the authors examined a series of changes in free energy inputs and how these have altered global material cycles. On the basis of their analyses, they conclude that human sustainability will not only require a shift from fossil fuel to solar power, but also a far more active effort to recycle materials such as metals.

Here, I have taken a more bottom-up approach. In considering expansions in the types of energy underpinning the biosphere, I have sought to describe the step-wise construction of a life–planet system. Using energy expansions as the lens reveals a fundamental, recursive interplay between events in the evolution of life and the development of the planetary environment. From this viewpoint, a number of insights emerge.

First, increasing the types of energy sources available to life has led to a far more complex biosphere. Although only geochemical energy and sunlight can power the de novo transformation of inorganic carbon into living tissue, the complexity of the current biosphere rests on multiple levels of energy use. Cyanobacteria, for instance, often require the presence of non-light-using consort organisms in order to grow well141,​142,​143. Conversely, owing to the metabolic capacities of their prokaryotic symbionts and endosymbionts, eukaryotes are able to live in a far wider range of environments than they could otherwise access82. The step-wise diversification of the biosphere has, in turn, led to an expansion of possible niches, from more complex microbial mats to old shells and abandoned burrows. At the same time, the capacity of life to impact the planetary environment—and thereby the environment in which future life will evolve—has expanded dramatically with each epoch.

Because the construction of the biosphere has depended on these energy expansions, the vanishing of an energy source, even temporarily, could cause a corresponding contraction in the biosphere. In the context of the Phanerozoic, some authors have attributed large-scale patterns of both biospheric expansion and contraction to corresponding fluctuations in oxygen availability, with expanding ocean anoxia corresponding to mass extinction events (end-Permian144,145; end Triassic146). Likewise, Krin147 has suggested that one factor in the mass extinction at the end of the Cretaceous may have been dust ejected by the Chicxulub asteroid impact, which may have blocked out the sun long enough to cause a global collapse in photosynthesis. Quantifying this pattern further would be an interesting line for future research.

A related avenue for future research would be an examination of macroevolutionary trends of energy use. For example, Vermeij148 argued that the Phanerozoic has been characterized by the repeated replacement of low-energy life forms by those able to harness larger amounts of energy. Among the trends he identified were endotherms tending to replace ectotherms, and angiosperms tending to replace gymnosperms. (The lower-energy form does not always become extinct; sometimes its range is just restricted to a low-energy environment.) Investigating this trend for earlier epochs—or even applying it to human societies149—might be enlightening.

A second insight that emerges from this Perspective is that the two clear inflection points in the history of Earth—the Great Oxidation Event and the emergence of mobile animals—also coincide with expansions in the kinds of energy sources available to, and consumed by, living beings. The Great Oxidation shifted the prevailing chemistry of the atmosphere and upper ocean and made oxygen gas abundant. The emergence of life forms that eat one another transformed the nature of ecosystems, and introduced a powerful new set of evolutionary interactions, thus accelerating the pace of macroevolutionary change. From this point of view, the familiar observation that Earthly life is powered by the sun takes on a more nuanced aspect: the modern biosphere is powered not merely by sunshine but by the oxygen that results from using sunshine in a particular way.

This Perspective further suggests that, through the harnessing of fire as a source of energy, Earth has now arrived at a new inflection point. Considering life–Earth history through the lens of energy expansions supports the view that the Anthropocene is a genuinely novel phase of the planet's geological and biological development—a conclusion independently reached by Lenton and colleagues7. The technology of fire may also, perhaps, mark an inflection point for the Solar System and beyond. Spacecraft from Earth may, intentionally or not, take Earthly life to other celestial objects (though whether any Earthly life forms can thrive elsewhere remains unknown).

As this is the only life–planet system we currently know of, it is impossible to know how representative it is of life–planet systems in general. But if the development of other life–planet systems requires a similar series of energy expansions, the framework presented here suggests a way to anticipate the paths that such systems might take. For instance, if a planet has only geochemical energy—perhaps because it is far from its star, or because it is a nomad150,151 and has no star at all—any life present may have “a limited future in terms of the heights it could achieve”152. Or suppose a planet is unable to accumulate oxygen. This could happen if living organisms never evolve a way of splitting water to produce the gas in the first place6,153; but even if they do, the planet itself may have characteristics that prevent oxygen from ever building up6,66. Without oxygen, the geological, ecological and evolutionary potential of a life–planet system is likely to be constrained, even if life forms analogous to eukaryotes in their energy-harnessing power (Box 2) were to evolve. Conversely, some planets might be able to accumulate new forms of energy, and life forms able to take advantage of them, much faster than Earth has66.

In short, this Perspective of energy expansions suggests that the likely development of a life–planet system will depend on the interplay between the planet's cosmic situation, its intrinsic properties, and the paths that evolving life can potentially take. The example of this life–planet system suggests that the development of a flourishing, complex biosphere depends on a virtuous circle between evolving life forms and transformations of their planetary home.

Additional information

How to cite this article: Judson, O. P. The energy expansions of evolution. Nat. Ecol. Evol. 1, 0138 (2017).

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    , & Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, 100–180 (1977).

  2. 2.

    & Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25, 175–243 (2001).

  3. 3.

    La Biosphère (Félix Alcan, 1929).

  4. 4.

    Atmospheric and hydrospheric evolution on the primitive earth. Science 160, 729–736 (1968).

  5. 5.

    General Energetics: Energy in the Biosphere and Civilization (John Wiley and Sons, 1991).

  6. 6.

    & Revolutions that Made the Earth (Oxford Univ. Press, 2011).

  7. 7.

    , & Revolutions in energy input and material cycling in Earth history and human history. Earth Syst. Dynam. 7, 353–370 (2016).

  8. 8.

    , , & Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types. Geochim. Cosmochim. Acta 75, 5736–5748 (2011).

  9. 9.

    , , , & Hydrogen generation from low-temperature water–rock reactions. Nat. Geosci. 6, 478–484 (2013).

  10. 10.

    & Serpentinites, hydrogen, and life. Elements 9, 129–134 (2013).

  11. 11.

    , , & Pathways for abiotic organic synthesis at submarine hydrothermal fields. Proc. Natl Acad. Sci. USA 112, 7668–7672 (2015).

  12. 12.

    , & Serpentinization as a source of energy at the origin of life. Geobiology 8, 355–371 (2010).

  13. 13.

    , & How did LUCA make a living? Chemiosmosis in the origin of life. BioEssays 32, 271–280 (2010).

  14. 14.

    , , , & The role of energy in the emergence of biology from chemistry. Orig. Life Evol. Biosph. 42, 459–468 (2012).

  15. 15.

    et al. Early bioenergetic evolution. Phil. Trans. R. Soc. Lond. B 368, 20130088 (2013).

  16. 16.

    et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).

  17. 17.

    & The stepwise evolution of early life driven by energy conservation. Mol. Biol. Evol. 23, 1286–1292 (2006).

  18. 18.

    13C-depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from west Greenland. Science 283, 674–676 (1999).

  19. 19.

    et al. Atmospheric hydrogen peroxide and Eoarchean iron formations. Geobiology 13, 1–14 (2015).

  20. 20.

    , , & Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon. Proc. Natl Acad. Sci. USA 112, 14518–14521 (2015).

  21. 21.

    , , , & Rapid emergence of life shown by discovery of 3,700-million-year-old microbial structures. Nature 537, 535–538 (2016).

  22. 22.

    et al. Evidence for early life in Earth's oldest hydrothermal vent precipitates. Nature 543, 60–64 (2017).

  23. 23.

    Mineral environments on the earliest Earth. Elements 6, 25–30 (2010).

  24. 24.

    , & On the origin of heterotrophy. Trends Microbiol. 24, 12–25 (2016).

  25. 25.

    in Treatise on Geochemistry 2nd edn (eds Holland, H. & Turekian, K.) 6, 177–195 (Elsevier, 2014).

  26. 26.

    & Archaean metabolic evolution of microbial mats. Proc. R. Soc. Lond. B 266, 2375–2382 (1999).

  27. 27.

    , , & Physiological differentiation within a single-species biofilm fueled by serpentinization. mBio 2, e00127–11 (2011).

  28. 28.

    Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262–280 (1997).

  29. 29.

    & Life: past, present and future. Phil. Trans. R. Soc. Lond. B 354, 1923–1939 (1999).

  30. 30.

    & Ecology and Evolution in Anoxic Worlds (Oxford Univ. Press, 1995).

  31. 31.

    & The origin of viruses. Res. Microbiol. 160, 466–472 (2009).

  32. 32.

    , & A coupled atmosphere–ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005).

  33. 33.

    , & Early anaerobic metabolisms. Phil. Trans. R. Soc. Lond. B 361, 1819–1836 (2006).

  34. 34.

    & Niches of the pre-photosynthetic biosphere and geologic preservation of Earth's earliest ecology. Geobiology 5, 101–117 (2007).

  35. 35.

    , & Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44, 647–683 (2016).

  36. 36.

    & Hydrogen-based carbon fixation in the earliest known photosynthetic organisms. Geology 34, 37–40 (2006).

  37. 37.

    & Evolution of photosynthesis. Annu. Rev. Plant Biol. 62, 515–548 (2011).

  38. 38.

    Photoheterotrophy in marine prokaryotes. J. Plankton Res. 31, 933–938 (2009).

  39. 39.

    , & A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites. Geobiology 5, 119–126 (2007).

  40. 40.

    , , , & Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature 440, 516–519 (2006).

  41. 41.

    & Processes on the young Earth and the habitats of early Life. Annu. Rev. Earth Planet. Sci. 40, 521–549 (2012).

  42. 42.

    & Earth and Mars: evolution of atmospheres and surface temperatures. Science 177, 52–56 (1972).

  43. 43.

    , , & A revised, hazy methane greenhouse for the Archean Earth. Astrobiology 8, 1127–1137 (2008).

  44. 44.

    & How Earth's atmosphere evolved to an oxic state: a status report. Earth Planet. Sci. Lett. 237, 1–20 (2005).

  45. 45.

    Radiolysis of water: a look at its origin and occurrence in the nature. Radiat. Phys. Chem. 72, 181–186 (2005).

  46. 46.

    et al. Dating the rise of atmospheric oxygen. Nature 427, 117–120 (2004).

  47. 47.

    , & The rise of oxygen in Earth's early ocean and atmosphere. Nature 506, 307–315 (2014).

  48. 48.

    , & The role of biology in planetary evolution: cyanobacterial primary production in low-oxygen Proterozoic oceans. Environ. Microbiol. 18, 325–340 (2016).

  49. 49.

    The problem of the Precambrian atmosphere. S. Afr. J. Sci. 24, 155–172 (1927).

  50. 50.

    , , & The evolutionary diversification of cyanobacteria: molecular–phylogenetic and paleontological perspectives. Proc. Natl Acad. Sci. USA 103, 5442–5447 (2006).

  51. 51.

    , , & Morphological record of oxygenic photosynthesis in conical stromatolites. Proc. Natl Acad. Sci. USA 106, 10939–10943 (2009).

  52. 52.

    , & Geological constraints on the origin of oxygenic photosynthesis. Photosynth. Res. 107, 11–36 (2011).

  53. 53.

    What caused the rise of atmospheric O2? Chem. Geol. 362, 13–25 (2013).

  54. 54.

    , & Bistability of atmospheric oxygen and the Great Oxidation. Nature 443, 683–686 (2006).

  55. 55.

    , , & Composition and structure of microbial communities from stromatolites of Hamelin Pool in Shark Bay, Western Australia. Appl. Environ. Microbiol. 71, 4822–4832 (2005).

  56. 56.

    , & Geochemical evidence for terrestrial ecosystems 2.6 billion years ago. Nature 408, 574–578 (2000).

  57. 57.

    , & Contributions to late Archaean sulphur cycling by life on land. Nat. Geosci. 5, 722–725 (2012).

  58. 58.

    & Evolution of a habitable planet. Annu. Rev. Astron. Astrophys. 41, 429–463 (2003).

  59. 59.

    , & Biogeochemical modelling of the rise in atmospheric oxygen. Geobiology 4, 239–269 (2006).

  60. 60.

    & The Great Oxidation Event and mineral diversification. Elements 6, 31–36 (2010).

  61. 61.

    et al. Mineral evolution. Am. Mineral. 93, 1693–1720 (2008).

  62. 62.

    et al. Aerobically respiring prokaryotic strains exhibit a broader temperature-pH-salinity space for cell division than anaerobically respiring and fermentative strains. J. R. Soc. Interface 12, 20150658 (2015).

  63. 63.

    et al. in Reading the Archive of Earth's Oxygenation (eds Melezhik, V. A. et al.) 1059–1109 (Springer, 2013).

  64. 64.

    , & The loss of mass-independent fractionation in sulfur due to a Palaeoproterozoic collapse of atmospheric methane. Geobiology 4, 271–283 (2006).

  65. 65.

    & The effect of widespread early aerobic marine ecosystems on methane cycling and the Great Oxidation. Earth Planet. Sci. Lett. 434, 42–51 (2016).

  66. 66.

    , , & Why O2 is required by complex life on habitable planets and the concept of planetary “oxygenation time”. Astrobiology 5, 415–438 (2005).

  67. 67.

    , & Availability of O2 and H2O2 on pre-photosynthetic Earth. Astrobiology 11, 293–302 (2011).

  68. 68.

    , & Quantifying the areal extent and dissolved oxygen concentrations of Archean oxygen oases. Chem. Geol. 362, 35–43 (2013).

  69. 69.

    & Biogeochemical transformations in the history of the ocean. Annu. Rev. Mar. Sci. 9, 31–58 (2017).

  70. 70.

    , & Reactive oxygen intermediates in biochemistry. Annu. Rev. Biochem. 55, 137–166 (1986).

  71. 71.

    The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11, 443–454 (2013).

  72. 72.

    Oxygen-collagen priority and the early metazoan fossil record. Proc. Natl Acad. Sci. USA 65, 781–788 (1970).

  73. 73.

    , , & An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 (2013).

  74. 74.

    , & Endosymbiotic theories for eukaryote origin. Phil. Trans. R. Soc. Lond. B 370, 20140330 (2015).

  75. 75.

    The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant Biol. 64, 583–607 (2013).

  76. 76.

    Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386–404 (2000).

  77. 77.

    Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6, a016121 (2014).

  78. 78.

    et al. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444–495 (2012).

  79. 79.

    & The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).

  80. 80.

    & The rise of oxygen and complex life. J. Eukaryot. Microbiol. 59, 111–113 (2012).

  81. 81.

    & The energetics of genome complexity. Nature 467, 929–934 (2010).

  82. 82.

    Symbiosis as a general principle in eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6, a016113 (2014).

  83. 83.

    , , & The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009).

  84. 84.

    The Ediacara biota: Neoproterozoic origin of animals and their ecosystems. Annu. Rev. Earth Planet. Sci. 33, 421–442 (2005).

  85. 85.

    et al. Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. Proc. Natl Acad. Sci. USA 106, 24–27 (2009).

  86. 86.

    An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proc. Natl Acad. Sci. USA 70, 1486–1489 (1973).

  87. 87.

    Macroevolution and macroecology through deep time. Palaeontology 50, 41–55 (2007).

  88. 88.

    Origins and early evolution of predation. Paleontol. Soc. Papers 8, 289–318 (2002).

  89. 89.

    & Testate amoebae in the Neoproterozoic Era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon. Paleobiology 26, 360–385 (2000).

  90. 90.

    The rise of predators. Geology 39, 607–608 (2011).

  91. 91.

    & Scale microfossils from the mid-Neoproterozoic Fifteenmile Group, Yukon Territory. J. Paleontol. 86, 775–800 (2012).

  92. 92.

    & in Multicellularity: Origins and Evolution (eds Niklas, K. J. & Neumann, S. D.) 3–16 (MIT Press, 2016).

  93. 93.

    The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235–251 (2008).

  94. 94.

    et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

  95. 95.

    , , & Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624–13629 (2011).

  96. 96.

    , , , & The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Funct. Ecol. 19, 291–298 (2005).

  97. 97.

    The paradox of the plankton. Am. Nat. 95, 137–145 (1961).

  98. 98.

    & Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction. Biol. Conserv. 145, 205–213 (2012).

  99. 99.

    Animals and the invention of the Phanerozoic Earth system. Trends Ecol. Evol. 26, 81–87 (2011).

  100. 100.

    The origin of skeletons. Palaios 4, 585–589 (1989).

  101. 101.

    Mesozoic radiolarites–accumulation as a function of sea surface fertility on Tethyan margins and in ocean basins. Sedimentology 60, 292–318 (2013).

  102. 102.

    Towards an unbiased estimate of fluctuations in reef abundance and volume during the Phanerozoic. Biogeosciences 3, 15–27 (2006).

  103. 103.

    & Patterns in bioclastic accumulation through the Phanerozoic: Changes in input or in destruction? Geology 22, 1139–1143 (1994).

  104. 104.

    Influence of seawater chemistry on biomineralization throughout Phanerozoic time: Paleontological and experimental evidence. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 214–236 (2006).

  105. 105.

    , & Secular change in chert distribution: a reflection of evolving biological participation in the silica cycle. Palaios 4, 519–532 (1989).

  106. 106.

    & in Coccolithophores: From Molecular Processes to Global Impact (eds Thierstein, H. R. & Young, J. R.) 99–125 (Springer, 2004).

  107. 107.

    & Role of large particles in the transport of elements and organic compounds through the oceanic water column. Prog. Oceanog. 16, 147–194 (1986).

  108. 108.

    et al. Iron defecation by sperm whales stimulates carbon export in the Southern Ocean. Proc. R. Soc. Lond. B 277, 3527–3531 (2010).

  109. 109.

    The biogeochemistry of vertebrate excretion. Bull. Am. Mus. Nat. Hist. 96, 1–554 (1950).

  110. 110.

    & When life got smart: the evolution of behavioral complexity through the Ediacaran and early Cambrian of NW Canada. J. Paleontol. 88, 309–330 (2014).

  111. 111.

    The Formation of Vegetable Mould, Through the Action of Worms, with Observations on Their Habits (John Murray, 1881).

  112. 112.

    & Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proc. Natl Acad. Sci. USA 106, 8123–8127 (2009).

  113. 113.

    et al. Stabilization of the coupled oxygen and phosphorus cycles by the evolution of bioturbation. Nat. Geosci. 7, 671–676 (2014).

  114. 114.

    , , & Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376, 53–56 (1995).

  115. 115.

    et al. Global frequency and distribution of lightning as observed from space by the Optical Transient Detector. J. Geophys. Res. 108, 4005 (2003).

  116. 116.

    , & Lightning and lightning fire, central cordillera, Canada. Int. J. Wildland Fire 11, 41–51 (2002).

  117. 117.

    New results on planetary lightning. Adv. Space Res. 50, 293–310 (2012).

  118. 118.

    & Limits for combustion in low O2 redefine paleoatmospheric predictions for the Mesozoic. Science 321, 1197–1200 (2008).

  119. 119.

    , , , & Baseline intrinsic flammability of Earth's ecosystems estimated from paleoatmospheric oxygen over the past 350 million years. Proc. Natl Acad. Sci. USA 107, 22448–22453 (2010).

  120. 120.

    , & Charcoal in the Silurian as evidence for the earliest wildfire. Geology 32, 381–383 (2004).

  121. 121.

    , , , & Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16, 406–411 (2011).

  122. 122.

    , & The global distribution of ecosystems in a world without fire. New Phytol. 165, 525–538 (2005).

  123. 123.

    & Fire and the spread of flowering plants in the Cretaceous. New Phytol. 188, 1137–1150 (2010).

  124. 124.

    , , , & Phylogeny of the ants: diversification in the age of angiosperms. Science 312, 101–104 (2006).

  125. 125.

    & Bees diversified in the age of eudicots. Proc. R. Soc. Lond. B 280, 20122686 (2012).

  126. 126.

    et al. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483, 457–460 (2013).

  127. 127.

    in Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. Belcher, C. M.) 289–308 (John Wiley and Sons, 2013).

  128. 128.

    , , , & The raw and the stolen: cooking and the ecology of human origins. Curr. Anthropol. 40, 567–594 (1999).

  129. 129.

    & Earliest fire in Africa: towards the convergence of archaeological evidence and the cooking hypothesis. Azania 48, 5–30 (2013).

  130. 130.

    , & Energetic consequences of thermal and nonthermal food processing. Proc. Natl Acad. Sci. USA 108, 19199–19203 (2011).

  131. 131.

    , & Cooking increases net energy gain from a lipid-rich food. Am. J. Phys. Anthropol. 156, 11–18 (2015).

  132. 132.

    Elements of Physical Biology (Williams and Wilkins, 1925).

  133. 133.

    Enriching the Earth (MIT Press, 2001).

  134. 134.

    , , , & How a century of ammonia synthesis changed the world. Nat. Geosci. 1, 636–639 (2008).

  135. 135.

    et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752 (2014).

  136. 136.

    Singularities (Cambridge Univ. Press, 2005).

  137. 137.

    & Directionality in the history of life: diffusion from the left wall or repeated scaling of the right? Paleobiology 26, 1–14 (2000).

  138. 138.

    & The Major Transitions in Evolution (WH Freeman, 1995).

  139. 139.

    Toward major evolutionary transitions theory 2.0. Proc. Natl Acad. Sci. USA 112, 10104–10111 (2015).

  140. 140.

    & (eds) The Major Transitions in Evolution Revisited (MIT Press, 2011).

  141. 141.

    , , , & Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by ‘helper’ heterotrophic bacteria. Appl. Environ. Microbiol. 74, 4530–4534 (2008).

  142. 142.

    Interaction between cyanobacteria and aerobic heterotrophic bacteria in the degradation of hydrocarbons. Int. Biodeter. Biodegr. 64, 58–64 (2010).

  143. 143.

    , , , & Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshwater Biol. 56, 1065–1080 (2011).

  144. 144.

    & How to kill (almost) all life: the end-Permian extinction event. Trends Ecol. Evol. 18, 358–365 (2003).

  145. 145.

    et al. Anoxia/high temperature double whammy during the Permian–Triassic marine crisis and its aftermath. Sci. Rep. 4, 4132 (2014).

  146. 146.

    et al. Episodic photic zone euxinia in the northeastern Panthalassic Ocean during the end-Triassic extinction. Geology 43, 307–310 (2015).

  147. 147.

    The Chicxulub impact event and its environmental consequences at the Cretaceous–Tertiary boundary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 255, 4–21 (2007).

  148. 148.

    Inequality and the directionality of history. Am. Nat. 153, 243–253 (1999).

  149. 149.

    Energy in Nature and Society: General Energetics of Complex Systems (MIT Press, 2008).

  150. 150.

    Life-sustaining planets in interstellar space? Nature 400, 32 (1999).

  151. 151.

    , , & Nomads of the Galaxy. Mon. Not. R. Astron. Soc. 423, 1856–1865 (2012).

  152. 152.

    , & Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? Trends Microbiol. 13, 405–410 (2005).

  153. 153.

    Implications of an anthropic model of evolution for emergence of complex life and intelligence. Astrobiology 8, 175–185 (2008).

  154. 154.

    & Catalytic proficiency: the unusual case of OMP decarboxylase. Annu. Rev. Biochem. 71, 847–885 (2002).

  155. 155.

    , , , & Role of microbes in the smectite-to-illite reaction. Science 303, 830–832 (2004).

  156. 156.

    , & Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503–537 (1989).

  157. 157.

    Carbon isotopes as biogeochemical recorders of life over 3.8 Ga of Earth history: evolution of a concept. Precambrian Res. 106, 117–134 (2001).

  158. 158.

    The function of genomes in bioenergetic organelles. Phil. Trans. R. Soc. Lond. B 358, 19–38 (2003).

  159. 159.

    et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642 (2010).

  160. 160.

    & Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl Acad. Sci. USA 99, 3695–3700 (2002).

  161. 161.

    Cost-minimization of amino acid usage. J. Mol. Evol. 56, 151–161 (2003).

  162. 162.

    Selection on synthesis cost affects interprotein amino acid usage in all three domains of life. J. Mol. Evol. 64, 558–571 (2007).

  163. 163.

    & Selection costs of amino acid substitutions in ColE1 and ColIa gene clusters harbored by Escherichia coli. Mol. Biol. Evol. 15, 774–776 (1998).

  164. 164.

    & Oxygen and animal evolution: did a rise of atmospheric oxygen trigger the origin of animals? BioEssays 36, 1145–1155 (2014).

  165. 165.

    , , , & Of early animals, anaerobic mitochondria, and a modern sponge. BioEssays 36, 924–932 (2014).

  166. 166.

    et al. Oxygen, ecology, and the Cambrian radiation of animals. Proc. Natl Acad. Sci. USA 110, 13446–13451 (2013).

  167. 167.

    Oxygen as a prerequisite to the origin of the Metazoa. Nature 183, 1170–1172 (1959).

  168. 168.

    & Early animal evolution: emerging views from comparative biology and geology. Science 284, 2129–2137 (1999).

  169. 169.

    et al. Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nat. Commun. 6, 7142 (2015).

  170. 170.

    , , , & Earth's oxygen cycle and the evolution of animal life. Proc. Natl Acad. Sci. USA 113, 8933–8938 (2016).

  171. 171.

    , , , & Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265 (2014).

Download references

Acknowledgements

Many thanks to G. Carr, T. Carvalho, D. C. Catling, D. Haydon, T. Goldberg, P. Jarne, A. H. Knoll, E. Kroll, N. Judson, N. Lane, T. Lenormand, G. Lichfield, B. C. T. Mason, O. Morton, J. Rolff, J. Swire, and especially A. Courtiol for helpful discussions and for comments on an earlier draft of the manuscript. Many thanks to W. F. Martin and T. M. Lenton for insightful reviews that improved the manuscript. Figure 1 was drawn by graphic designer F. Zsolnai, many thanks.

Author information

Affiliations

  1. Freie Universität Berlin, Institute of Biology, Königin-Luise-Strasse 1-3, D-14195 Berlin, Germany.

    • Olivia P. Judson
  2. Imperial College London, Department of Life Sciences, Silwood Park Campus, Ascot SL5 7PY, UK.

    • Olivia P. Judson
  3. University of Glasgow, Institute of Biodiversity, Animal Health and Comparative Medicine, Glasgow G12 8QQ, UK.

    • Olivia P. Judson

Authors

  1. Search for Olivia P. Judson in:

Competing interests

The author declares no competing financial interests.

Corresponding author

Correspondence to Olivia P. Judson.