Chance and the origin of life

Random chemical reactions in the Earth's primitive hydrosphere could have generated no more than 200 bits of information, whereas the first Darwinian organism must have encoded about a million bits, and therefore could not have arisen by chance. This information gap is bridged by separating reproduction from organism, and postulating a reproductive chemical community that would generate information by proto-Darwinian evolution. The information content of the initial community could have been as low as 160 bits, and its evolution might have led to the first Darwinian cell.     

Saltational symbiosis

Symbiosis has long been associated with saltational evolutionary change in contradistinction to gradual Darwinian evolution based on gene mutations and recombination between individuals of a species, as well as with super-organismal views of the individual in contrast to the classical one-genome: one organism conception. Though they have often been dismissed, and overshadowed by Darwinian theory, suggestions that symbiosis and lateral gene transfer are fundamental mechanisms of evolutionary innovation are borne out today by molecular phylogenetic research. It is time to treat these processes as central principles of evolution.     

An evolutionary perspective on the systems of adaptive immunity

We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function‐based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to ‘learn’ by cumulative trial‐and‐error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher‐level units entail the suppression of selection at lower levels, Darwinian immunity re‐opens cell‐level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell‐level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re‐invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system – the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the ‘Big Bang’ of vertebrate immunity, arguing that its origin involved a ‘difficult’ (i.e. low‐probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.     

Towards a General Definition of Life

A new definition of life is proposed and discussed in the present article. It is formulated by modifying and extending NASA’s working definition of life, which postulates that life is a “self-sustaining chemical system capable of Darwinian evolution”. The new definition includes a thermodynamical aspect of life as a far from equilibrium system and considers the flow of information from the environment to the living system. In our derivation of the definition of life we have assumed the hypothesis, that during the emergence of life evolution had to first involve autocatalytic systems that only subsequently acquired the capacity of genetic heredity. The new proposed definition of life is independent of the mode of evolution, regardless of whether Lamarckian or Darwinian evolution operated at the origins of life and throughout evolutionary history. The new definition of life presented herein is formulated in a minimal manner and it is general enough that it does not distinguish between individual (metabolic) network and the collective (ecological) one. The newly proposed definition of life may be of interest for astrobiology, research into the origins of life or for efforts to produce synthetic or artificial life, and it furthermore may also have implications in the cognitive and computer sciences.

     

The remarkable discreteness of being

Life is a discrete, stochastic phenomenon: for a biological organism, the time of the two most important events of its life (reproduction and death) is random and these events change the number of individuals of the species by single units. These facts can have surprising, counterintuitive consequences. I review here three examples where these facts play, or could play, important roles: the spatial distribution of species, the structuring of biodiversity and the (Darwinian) evolution of altruistic behaviour.     

A theory for the origin of a self-replicating chemical system. I: Natural selection of the autogen from short,random oligomers

Summary A theory is described for the origin of a simple chemical system named an autogen, consisting of two short oligonucleotide sequences coding for two simple catalytic peptides. If the theory is valid, under appropriate conditions the autogen would be capable of self-reproduction in a truly genetic process involving both replication and translation. Limited catalytic ability, short oligomer sequences, and low selectivities leading to sloppy information transfer processes are shown to be adequate for the origin of the autogen from random background oligomers. A series of discrete steps, each highly probable if certain minimum requirements and boundary conditions are satisfied, lead to exponential increase in population of all components in the system due to autocatalysis and hypercyclic organization. Nucleation of the components and exponential increase to macroscopic amounts could occur in times on the order of weeks. The feasibility of the theory depends on a number of factors, including the capability of simple protoenzymes to provide moderate enhancements of the accuracies of replication and translation and the likelihood of finding an environment where all of the required processes can occur simultaneously. Regardless of whether or not the specific form proposed for the autogen proves to be feasible, the theory suggests that the first self-replicating chemical systems may have been extremely simple, and that the period of time required for chemical evolution prior to Darwinian natural selection may have been far shorter than generally assumed. Due to the short time required, this theory, unlike others on the origin of genetic processes, is potentially capable of direct experimental verification. A number of prerequisites leading up to such an experiment are suggested, and some have been fulfilled. If successful, such an experiment would be the first laboratory demonstration of the spontaneous emergence by natural selection of a genetic, self-replicating, and evolving molecular system, and might represent the first step in the prebiotic environment of true Darwinian evolution toward a living cell.     

The first cellular bioenergetic process: Primitive generation of a proton-motive force

Summary It is proposed that the energy-transducing system of the first cellular organism and its precursor was fueled by the oxidation of hydrogen sulfide and ferric sulfide to iron pyrites and two [H⁺] on the outside surface of a vesicle (the cell membrane), with the concomitant reduction of CO or CO₂ on the interior. The resulting proton gradient across the cell membrane provides a proton-motive force, so that a variety of kinds of work can be done. It is envisioned as providing a selective advantage for cells capable of harvesting this potential. The proposed reactants for these reactions are consistent with the predicted composition of the Earth's early environment. Modern-day homologs of the ancestral components of the energy-transducing system are thought to be membrane-associated ferredoxins for the extracellular redox reaction, carbon monoxide dehydrogenase for the carbon fixation reaction, and ATPase for the harvesting of the proton gradient. With a source of consumable energy, the cell could drive chemical reactions and transport events in such a way as to be exploited by Darwinian evolution.     

A theoretical approach to the large-scale evolution of multicellularity and cell differentiation

In contrast to Darwinian evolution in which organisms have been selected by the instantaneous judgment of advantage or disadvantage for a mutated gene, the large-scale evolution of multicellular organisms by drastic changes in their genomes to produce new genes is theoretically formulated on the basis of the new concept of ‘biological activity’. The ‘biological activity’ of an organism is a macroscopic quantity determined by its whole genome and the environment, consisting of three terms; the energy acquired from the outside, the energy stored in the form of bio-molecules, and the systematization of multicellularity as well as of organizing genes and their products. The acquired energy minus stored energy is lost as heat, and the entropy production by the heat must compensate for the entropy reduction owing to the systematization in the organism. Under the boundary determined by this thermodynamic law, the organisms, which experienced gene duplication to produce new genes for multicellularity and cell differentiation, first decline to be minor members in a population by the increase in the energy to be stored and by the advanced systematization of cell differentiation. If the acquired energy is raised by the cooperative action of newly differentiated cells with the pre-existing types of cells, however, the ‘biological activity’ of this new style of organism can be recovered. The new style of organism generated through this evolutionary process does not necessarily expel the old style of organism to extinction but can coexist by choosing different material and energy resources. Moreover, this theory of large-scale evolution not only explains the punctuated mode of evolution indicated by paleontology but also reproduces the divergence of body plans observed in Triploblastica and Tracheophyta.     

A New Criterion for Demarcating Life from Non-Life

Criteria for demarcating life from non-life are important for deciding whether new candidate systems, either discovered extraterrestrially or constructed in the laboratory, are genuinely alive or not. They are also important for understanding the origin of life and its evolution. Current criteria are either too restrictive or too extensive. The new criterion proposed here poses that a system is living when it is capable of utilizing active causation, at evolutionary or behavioural timescales. Active causation is produced when the organism uses an estimate of its own Darwinian fitness to modulate the variance of stochasticity that drives hereditary or behavioural changes. The changes are subsequently fed back to the fitness estimate and used in the next cycle of a feedback loop. The ability to use a self-estimated fitness in this way is an evolved property of the organism, and the way in which fitness is estimated is therefore controlled and stabilized by Darwinian evolution. The hereditary and behavioural trajectories resulting from this mechanism combine predictability with unpredictability, and the mechanism produces a form of self-directed agency in living organisms that is absent from non-living systems.     

Computer simulation of different types of evolutionary process

The computer model of two alternative variants of biological evolution is proposed. The first variant supposes random while the second--directed change of individual features, thus corresponding to the Darwinian and non-Darwinian evolution. The evolution of fish communities in fresh waters serves as a particular example. The model is executed using object-oriented method of programming and mathematical apparatus of fuzzy logics. The investigation of the model showed that process of Darwinian evolution is connected with significantly greater species diversity and variability of evolutionary process trajectories than non-Darwinian one. On the other hand, non-Darwinian type of evolution provides fast achievement of high individual fitness, especially under conditions of constant environment. Non-Darwinian type evolution failed in big evolutionary alteration (for example, transition to predation); while the Darwinian evolution under the same conditions can produce such alterations though it took more time and many extinct species. Phylogenetic tree of Darwinian evolution is always more complex than of non-Darwinian one under the same conditions.     

Is pre-Darwinian evolution plausible?

Background

This essay highlights critical aspects of the plausibility of pre-Darwinian evolution. It is based on a critical review of some better-known open, far-from-equilibrium system-based scenarios supposed to explain processes that took place before Darwinian evolution had emerged and that resulted in the origin of the first systems capable of Darwinian evolution. The researchers’ responses to eight crucial questions are reviewed. The majority of the researchers claim that there would have been an evolutionary continuity between chemistry and “biology”. A key question is how did this evolution begin before Darwinian evolution had begun? In other words the question is whether pre-Darwinian evolution is plausible.

Results

Strengths and weaknesses of the reviewed scenarios are presented. They are distinguished between metabolism-first, replicator-first and combined metabolism-replicator models. The metabolism-first scenarios show major issues, the worst concerns heredity and chirality. Although the replicator-first scenarios answer the heredity question they have their own problems, notably chirality. Among the reviewed combined metabolism-replicator models, one shows the fewest issues. In particular, it seems to answer the chiral question, and eventually implies Darwinian evolution from the very beginning. Its main hypothesis needs to be validated with experimental data.

Conclusion

From this critical review it is that the concept of “pre-Darwinian evolution” appears questionable, in particular because it is unlikely if not impossible that any evolution in complexity over time may work without multiplication and heritability allowing the emergence of genetically and ecologically diverse lineages on which natural selection may operate. Only Darwinian evolution could have led to such an evolution. Thus, Pre-Darwinian evolution is not plausible according to the author. Surely, the answer to the question posed in the title is a prerequisite to the understanding of the origin of Darwinian evolution.

Reviewers

This article was reviewed by Purificacion Lopez-Garcia, Anthony Poole, Doron Lancet, and Thomas Dandekar.

     

The relativity of Darwinian populations and the ecology of endosymbiosis

If there is a single discipline of science calling the basic concepts of biology into question, it is without doubt microbiology. Indeed, developments in microbiology have recently forced us to rethink such fundamental concepts as the organism, individual, and genome. In this paper I show how microorganisms are changing our understanding of natural aggregations and develop the concept of a Darwinian population to embrace these discoveries. I start by showing that it is hard to set the boundaries of a Darwinian population, and I suggest thinking of a Darwinian population as a relative property of a Darwinian individual. Then I argue, in contrast to the commonly held view, that Darwinian populations are multispecies units, and that in order to accept the multispecies account of Darwinian populations we have to separate fitness from natural selection. Finally, I show how all these ideas provide a theoretical framework leading to a more precise understanding of the ecology of endosymbiosis than is afforded by poetic metaphors such as ‘slavery’.     

Compositional complementarity and prebiotic ecology in the origin of life

We hypothesize that life began not with the first self-reproducing molecule or metabolic network, but as a prebiotic ecology of co-evolving populations of macromolecular aggregates (composomes). Each composome species had a particular molecular composition resulting from molecular complementarity among environmentally available prebiotic compounds. Natural selection acted on composomal species that varied in properties and functions such as stability, catalysis, fission, fusion and selective accumulation of molecules from solution. Fission permitted molecular replication based on composition rather than linear structure, while fusion created composomal variability. Catalytic functions provided additional chemical novelty resulting eventually in autocatalytic and mutually catalytic networks within composomal species. Composomal autocatalysis and interdependence allowed the Darwinian co-evolution of content and control (metabolism). The existence of chemical interfaces within complex composomes created linear templates upon which self-reproducing molecules (such as RNA) could be synthesized, permitting the evolution of informational replication by molecular templating. Mathematical and experimental tests are proposed.     

Chemical Ecology and Biomolecular Evolution

The belief in the Darwinian theory of evolution appeared to be shaken when one tried to interpret statements of molecular biology in it. As a consequence there arose a theory of non-Darwinian neutral evolution. The supporters of this theory believe that under natural conditions no factors exist which can distinguish and select organisms on their internal (molecular) structure. In the opinion of these neutralists natural selection cannot in principle control the molecular constitution of organisms. Contrary to the viewpoint of the critics of neutralism it is impossible to admit that nucleic acids, proteins and other biomolecules can evolve without the participation of natural selection. This controversy in contemporary theoretical biology can be solved by integrating the conceptions of molecular ecology with Darwinian theory. Molecular ecology acknowledges the interactions of organisms by means of chemical substances synthesized by them. Such chemical ecological factors play a leading part in the selective stages of biomolecular evolution. These diverse chemical ecological interrelations take place intensively when living beings interact with parasitic microbes.     

Secret life of plants: From memory to intelligence

Plants are able to perform photosynthesis and cannot escape from environmental stresses, so they therefore developed sophisticated, highly responsive and dynamic physiology. Others'' and our results indicate that plants solve their optimal light acclimation and immune defenses, photosynthesis and transpiration by a computational algorithm of the cellular automation. Our recent results however suggest that plants are capable of processing information encrypted in light intensity and in its energy. With the help of nonphotochemical quenching and photoelectrophysiological signaling (PEPS) plants are able to perform biological quantum computation and memorize light training in order to optimize their Darwinian fitness. Animals have their network of neuron synapses, electrophysiological circuits and memory, but plants have their network of chloroplasts connected by stromules, PEPS circuits transduced by bundle sheath cells and cellular light memory. It is suggested that plants could be intelligent organisms with much higher organism organization levels than it was thought before.Key words: excess excitation energy, cellular automation, cellular light memory, Darwinian fitness, nonphotochemical quenching, photoelectrophysiological signaling, SAA, SAR     

Extending and expanding the Darwinian synthesis: the role of complex systems dynamics

Darwinism is defined here as an evolving research tradition based upon the concepts of natural selection acting upon heritable variation articulated via background assumptions about systems dynamics. Darwin's theory of evolution was developed within a context of the background assumptions of Newtonian systems dynamics. The Modern Evolutionary Synthesis, or neo-Darwinism, successfully joined Darwinian selection and Mendelian genetics by developing population genetics informed by background assumptions of Boltzmannian systems dynamics. Currently the Darwinian Research Tradition is changing as it incorporates new information and ideas from molecular biology, paleontology, developmental biology, and systems ecology. This putative expanded and extended synthesis is most perspicuously deployed using background assumptions from complex systems dynamics. Such attempts seek to not only broaden the range of phenomena encompassed by the Darwinian Research Tradition, such as neutral molecular evolution, punctuated equilibrium, as well as developmental biology, and systems ecology more generally, but to also address issues of the emergence of evolutionary novelties as well as of life itself.     

A neutral theory of biogenesis

The selective Darwinian theory of chemical evolution is critically reviewed and the tentative conclusion is reached that neither the theoretical analyses nor the experiments with phages can really prove it. An alternative proposal is put forth which considers the possibility that the biogenetic process has been driven by stochastic forces, e.g. it took place in the absence of Darwinian selection which, in turn, started only when the first protocells came into existence. The dynamics of the early self-organization of living structures should be understood in terms of self-assembly. The complexification of living matter is thus not represented as a gradual phenomenon but as a series of abrupt and relatively fast transitions consisting in the aggregation of pre-systems which had evolved by their own. The shift towards new and variegated states proposed by the bifurcation theory are not considered particularly relevant for reasons reported in the text, nor is it believed that dissipation can entirely account for the order observed in living cells.     

New thoughts on the evolution of hormone-receptor systems

A possible pathway of the evolution of hormone-receptor systems has been discussed in light of the genomic potential hypothesis. Unlike the Darwinian system which is based on uninvestigatable chance events, the genomic potential hypothesis offers predictions based upon chemical determinism (boundary determinism). Accordingly, the production of highly specific protein-protein interactions between receptors and hormones, for example, are based upon the development of interacting components before the primordial chemistry was segregated by membranes. It is proposed that in addition to the primary structure (coding activity) a higher level of information exists in the genome which caused genomic products to function in a complementary fashion in living systems. The first steps in that direction have already been taken via experiments on sense and antisense peptides which may have specific relationships to each other. It is clear that I have not given an answer but I hope that I have touched upon certain aspects of a problem that can be illuminated better by a new and different approach to evolution. The hormone-receptor development was probably a powerful formative force in the development of macroorganisms, and its baffling complexity can only begin to find an explanation on the basis of structure/function relationships of the encoding material and its products.(ABSTRACT TRUNCATED AT 250 WORDS)     

Primeval cells: possible energy-generating and cell-division mechanisms

It is proposed that the first entity capable of adaptive Darwinian evolution consisted of a liposome vesicle formed of abiotically produced phospholipidlike molecules; a very few informational macromolecules; and some abiogenic, lipid-soluble, organic molecule serving as a symporter for phosphate and protons and as a means of high-energy-bond generation. The genetic material had functions that led to the production of phospholipidlike materials (leading to growth and division of the primitive cells) and of the carrier needed for energy transduction. It is suggested that the most primitive exploitable energy source was the donation of 2H+ + 2e- at the external face of the primitive cell. The electrons were transferred (by metal impurities) to internal sinks of organic material, thus creating, via a deficit, a protonmotive force that could drive both the active transport of phosphate and high-energy-bond formation. This model implies that proton translocation in a closed-membrane system preceded photochemical or electron transport mechanisms and that chemically transferable metabolic energy was needed at a much earlier stage in the development of life than has usually been assumed. It provides a plausible mechanism whereby cell division of the earliest protocells could have been a spontaneous process powered by the internal development of phospholipids. The stimulus for developing this evolutionary sequence was the realization that cellular life was essential if Darwinian "survival of the fittest" was to direct evolution toward adaptation to the external environment.     

Darwinian evolution in games with perfect information

We consider a model of Darwinian evolution in games with perfect information like chess or checkers. The evolution is viewed as a sequence of strategies, each of which wins over its immediate predecessor. We argue that the intelligence level of strategies need not necessarily increase during this type of evolution.