Before Darwin
How the earth went from lifeless to life.
Even as political rhetoric and court battles reflect a public struggle over Darwin's theory of evolution as an explanation for the origin of humans, a different struggle is unfolding within science about the adequacy of evolution as a theoretical foundation for biology. On the surface, the two debates seem to have little to do with one another, but in a subtle way both reflect the need for a richer theoretical biology. The perception of evolution among the wider public might even be improved by better communication of scientific concerns about the limitations of evolutionary theory, and how those concerns are being addressed.
A sympathetic reading of public distrust over evolution would be that a simple theory of change seems too bare to account for the richness of structure we see in the world around us, and for how that structure first came to form. This certainly indicates a failure to appreciate the complex origins of order, and most popular science writing on evolution has been devoted to explaining the surprising and delightful origins of eyes, wings, or peacock's tails. But besides this, an intuitive discomfort that a theory of change cannot adequately account for genuine novelty has a scientific counterpart. The original emergence of life from a lifeless geosphere is one of the most striking such cases.
While they share a certain level of unease, the public and scientific debates diverge sharply on how to overcome the limitations of evolutionary theory. Public rejections of Darwinian ideas are bound up with a wish to introduce something more complicated than undirected variation and brute selection: a creator or designer responsible for novelty and innovation. In science, we recognize that while evolutionary theory is limited, some of the limits concern its connection to simpler - not more complicated - scientific principles than those introduced by Darwin. The remarkable story that is emerging about the origin of life is that these simpler principles may account for aspects of the biosphere that are older even than the evolutionary era itself, and which tie life at its core to the geochemistry of the earth.
To understand the role and also the limitations of evolutionary thinking in biology, it is helpful to recall a little history. Biology as a unified science did not even exist until well into the 20th century. Before that time, only application domains were recognized: systematics, botany, morphology, ecology, paleontology, physiology, medicine, and so forth. Each of these fields had its own domain-specific knowledge and even some elements of theory. However, the possibility of an overarching theory for all of life was not central to any of them. When this situation changed, the change was not a result of new ideas, but rather of ideas that had already been current for nearly a century, and had gone unrecognized as a foundation for theoretical unity.
The two ideas that we now think of together as the "theory of evolution" were Gregor Mendel's conception of the gene, and Charles Darwin's model of natural selection. Mendel had argued 1 in 1865 that traits do not mix like paint when they are handed down from parents to offspring, but rather are shuffled like cards. The concept of the unmixable source of a trait (say, whether peas would be smooth or wrinkled) was given the name gene, and Mendel's important observation was that the particular forms of genes usually did not change as they were passed from parents to offspring. This kind of faithful inheritance of traits, and shuffling instead of mixing of genes, allows populations to preserve diversity, instead of washing all traits out to some average form.
Darwin contemporaneously (1859) 2 had argued that the infrequent variations that do occur as traits are passed from parent to offspring need not be directed in order to enable adaptation. The greater reproductive success of individuals with better-adapted traits would be sufficient to establish the favorable forms. Darwin called this process natural selection as a reference to the selection exercised deliberately by human breeders, and he recognized that variation is necessary to give either breeders or nature the raw material from which to create changes in form.
Mendel's heredity and Darwin's selection were not theoretically central to the many particular life sciences, and were not even linked to each other until they were brought together by several researchers in the 1930s and 1940s, into what Julian Huxley called the Modern Synthesis of evolutionary biology. 3 The key observation of the Modern Synthesis (as it is now known) was that Mendelian heredity preserves the diversity of forms available in a population, while Darwinian selection changes their frequency of occurrence. Together the ideas link variation on the short-term to change in average properties on the long term. This synthesis did not replace the domain-specific theory in many life sciences, and in many cases it did not significantly change how it was used. The Modern Synthesis proposed a way in which random variations, with no foresight, could systematically lead to population changes in a manner that made sense in each of these fields.
This theory of evolution is really a framework for thinking about change in the living world. It provides no specific guesses for the kinds of traits that may exist, no strong requirements or prohibitions on how they may interact to make a complex organism or ecosystem, and no commitments to how innovation can occur. Even the problem of how a differentiated population ultimately divides into two distinct species (posed in the title of Darwin's seminal work) 2 remains a major technical problem in evolutionary biology.
There is no reason to view Mendel's and Darwin's ideas as self-contained or complete for biology, in the sense that all needed principles of organization can be generated from these two ideas alone. What they provide is a new class of dynamics that is different from what had previously been considered in physics, chemistry, or engineering. While these ideas seem particularly suited to answering questions about life, they have also found their way into thinking about such diverse fields as economics and Internet security, so they are certainly not uniquely biological.
Darwin's ideas were controversial as soon as they were introduced, because he and his contemporaries appreciated (and he intended) that they separated the concept of "good design" (called adaptation in evolution) from a need for a designer. In the enthusiasm for this one point, many other equally important points about the principles of evolution have been glossed over, and their omission is starting to be felt in practical problems in biology. Both Darwin and Mendel, working more than 150 years ago, took as self-evident what constituted an individual organism, and with a little more care, which similar organisms constituted a species. They recognized that individuals reproduced similar types of individuals, apart from minor changes, and that birth and death of individuals marked the change of generations.
Today, as we consider more life forms and their interactions, and especially as we consider the origin of life from a lifeless geosphere, the situation is more complicated. When multiple strains of virus "mate" by coinfecting a host, many different notions of individual become blurred even within a single infected cell: the two viral strains that might insert genes into the host genome; the viral and host genomes that are both struggling to control the same cell's metabolism; and the host cell's participation in a larger organism. We have learned that quite distinct strains of bacteria and archaea routinely exchange genes, and they probably did so much more promiscuously in the earliest stages of cellular life than they do today. Thus, the genetic and metabolic notions of individuality become even more loosely bound, and the concept of species becomes extremely problematic. These examples, and many others as well, illustrate that the concepts that Mendel and Darwin took as the starting points for their science may not apply to all biological situations. Indeed, even when they do apply, they must be explained within the context of a larger science.
We can identify four assumptions that must be made for evolutionary ideas to be even expressible, and we can then ask what science must be done to justify these assumptions, in particular for the first emergence of life.
Traditionally in physics and chemistry, preparing an experiment in the same way twice was expected to lead to the same outcome, as a criterion for asking well-posed questions. A feature that makes biology a fundamentally new science is that "replaying the tape" of life would, in many important respects, not lead to the animals and plants we see in the world today. 4 If the nature of life did not permit such variation, it would not have been possible for Mendel's peas to take either smooth or wrinkled forms, while remaining parts of viable pea plants. The fact that smooth or wrinkled variants could be passed down through heredity, without quickly reverting to a single form, meant that the form of each new generation was contingent on the form of its parents; that is, random variations in the past potentially could be preserved in populations for long stretches of time. Evolution can occur only when variations can arise and be preserved in this way.
Of course, heredity requires not only the possibility for variants to persist; it also requires a way that the features of the parent can be remembered and passed down, and this is the role of DNA and RNA, the carriers of Mendel's genetic information. The memory of life works so spectacularly well that it is often forgotten in biology just how difficult it is to produce a material that can remember anything, let alone remember it for billions of years as life has remembered many details of cellular structure and function. Yet the material of cells is not different from the material of the nonliving world except in its arrangement, and it is well understood in physics that arrangements constantly decay due to thermal jittering and other shocks. Some of the most sophisticated ideas in the field of condensed-matter physics concern the making of materials such as magnets, whose order is self-reinforcing over long times, allowing them to form memory devices.
Memory alone is not enough for evolution to occur. Unless different genomes could reliably create different kinds of organisms and ways of life, the remembered variations could not be submitted to natural selection for comparison and judgment. But any controller, including a genome, must first have autonomy from the thing controlled (the definition of control is that instructions mostly flow in one direction), leaving the controller somewhat detached from feedback about the consequences of its actions. When the components of the controller themselves fluctuate, wear out, or fail, it becomes capable of unfettered mistakes, and all human-designed control systems ultimately rely on intervention from the human world to repair and re-align them. Yet within life, control mechanisms have not only spontaneously emerged; they are self-sustaining within the enclosed system of the biosphere.
The reason it is possible for Mendelian heredity to preserve variation, and for Darwinian selection to act on it, is that traits do not mix continuously like colors of paint. At the same time, traits are not inherited independently. The many variable features of an organism are reproduced as a package if the organism successfully reproduces, and they are lost as a package when it dies. The granular nature of both traits and the individuals in which they are aggregated make selection a very complex mathematical process. Moreover, as we saw above, many different ways of collecting traits together in individuals exist, each with different dynamics. Yet at the same time, new forms of individuality are rare, suggesting that there are stark limits to how traits may be bound together in an organism while preserving in it the ability to evolve. 5
In physics and chemistry, none of these four features is a common occurrence, and yet evolution presupposes all of them. If life began in a physical world where none of them was present, we must first understand how and why they came into existence, before we can apply evolutionary ideas to study their subsequent change and refinement. Some modern studies of the origin of life 6 are addressing these older problems of emergence and looking for mechanisms that were predominant before Mendelian/Darwinian evolution was possible. The possibility that these mechanisms were simpler than evolutionary mechanisms also suggests that they are more robust, and that the order they initiated may still be observable in the organization of the biosphere today.
How does such a change in theoretical perspective lead us to reexamine the order in the biosphere? For one thing, if we do not assume the primacy of individuals, we notice that the strongest regularities of modern life cannot be seen in individual traits, but only at an ecological level of organization. 6 Here we find a common set of reactions for the synthesis of biological molecules that is universal throughout the biosphere and across the whole history of life. The stability and invariance of metabolic pathways gives them the appearance of features of the geosphere rather than of anything that depends on memory or control by individuals.
One of the most primitive functions life must perform lies at the very core of metabolism: It is the capture of carbon from environmental carbon dioxide (CO 2), which was abundant in the prebiotic era, and its synthesis into the backbones from which the rest of biomolecules are made. An amazing, small cycle of only 11 simple molecules, known as the reductive citric acid cycle, is capable of performing this feat. Some version of the reactions in this cycle is the foundation for biosynthesis in every kind of ecosystem on earth.
The cycle's basic function is to access otherwise inert CO 2, combine the carbon with electrons, and make molecules capable of repeating this reaction. The reaction sequence has the remarkable property that any molecule in the cycle, by accreting CO 2 to become longer and then splitting into two, reproduces a second copy of the same molecule while returning the first copy. Thus, like compound interest, it grows and draws diffuse carbon into a very specific pathway. The mathematics of energy and carbon that flow through this cycle resembles the mathematics that drive a hurricane to become the major transporter of moisture and energy over the oceans where it forms (see Figure below).
Carbon fixation is one of the most conserved reactions throughout the biosphere. It suggests that a bridge between geochemistry and life may be found in the mechanisms of metabolism and the principles of ecology, not in compartments or memory molecules, which could have come later. A metabolic organization capable of serving as such a bridge, however, could not have come from just any old network of organic chemical reactions. It would need to have been: 1) sparse within the network of possible reactions so that a few molecules were created in large supply, rather than a huge diversity of one-off molecules arising happenstance (which could not be assembled into anything); 2) particular, in that the pathways observed should be necessary and predictable, rather than accidents (which would depend on later memory mechanisms to be preserved), and 3) robust under jittering of the components, to permit later molecular memory systems to emerge using them as foundations. These principles can be used to find other primal reactions.
If the biosphere emerged through the self-organization of a metabolic system, like the citric acid cycle, the later formation of individuals would be understandable as solving a different problem of packaging. Distinct species can make up an ecosystem by partitioning metabolic tasks to become complementary specialists, but only if they solve the complex problems of obtaining the resources they do not make and settling into a balanced flow of resources among all the members of the ecosystem.
This view of the origins of life changes our understanding of the biosphere today in two ways. First, ecological principles become the foundations for the rest of biology, rather than merely secondary consequences of relations among individuals. Second, we should be warned that when we act as engineers in the living world, imagining that we can manipulate properties of individuals but remain ignorant of principles of ecology, we should expect the biosphere's response to be complex and not necessarily in accordance with our designs. The rapidly rising cost of industrial agriculture, and its fragility to shocks in energy supply, to pests, and to weather, is directly tied to the loss of natural ecological sources of stability in industrially managed agricultural systems.
When we consider what would be required for metabolism to have self-organized without supervision, we realize there is a rich, hierarchical, modular structure of the extant metabolism of the biosphere that looks far from accidental. The functions that particular chemicals fulfill, in the context of both the network and the constraints of the geochemical environment, suggest that the presence of these chemicals as a foundation for life may be required from first principles.
Many of the biological amino acids have simple and perhaps inevitable synthetic pathways starting from citric acid cycle backbones. Phosphorus, the element responsible for the assembly of large biomolecules by polymerization of small ones, naturally leads through a range of intermediate-sized compounds (technically termed cofactors, but we know many of them as the vitamins), which are central to molecular assembly and catalysis throughout metabolism. Even the genetic code, a master instruction set for the translation of RNA memory into protein control, has regularities that may be of precellular chemical origin. 7
Perhaps the most important feature of a chemical logic for metabolism on the early earth is that such a logic would not have become irrelevant when memory and control arose. More likely, it determined easy paths for biosynthesis, and gave fitness advantages to organisms that used them, over organisms that attempted to deviate too strongly. Thus we should not be surprised that modern life continues to respect an organization that first came about in the geosphere6.
The observations turned up in this way of asking about origins are ordinary enough, but they suggest a conceptual framework for biology that extends well beyond the classical theory of evolution, not only for the origin of life, but for its organization at all times. By drawing inputs from the many theoretical sciences that bear on the transition from lifeless to living matter, and in the process embedding biology more thoroughly in the framework of the other natural sciences, we learn that the required other origins of order may be simpler than the Darwinian paradigm, not more complex.
If public discontent with classical evolution as an inclusive theory stems partly from an intuitive appreciation of its limits, perhaps we as scientists can accomplish more by discussing how these limits are considered scientifically than by downplaying them.
Eric Smith is a professor at the Santa Fe Institute.