Kinetics and coexistence of autocatalytic reaction cycles.

Biological reproduction rests ultimately on chemical autocatalysis. Autocatalytic chemical cycles are thought to have played an important role in the chemical complexification en route to life. There are two, related issues: what chemical transformations allow such cycles to form, and at what speed they are operating. Here we investigate the latter question for solitary as well as competitive autocatalytic cycles in resource-unlimited batch and resource-limited chemostat systems. The speed of growth tends to decrease with the length of a cycle. Reversibility of the reproductive step results in parabolic growth that is conducive to competitive coexistence. Reversibility of resource uptake also slows down growth. Unilateral help by a cycle of its competitor tends to favour the competitor (in effect a parasite on the helper), rendering coexistence unlikely. We also show that deep learning is able to predict the outcome of competition just from the topology and the kinetic rate constants, provided the training set is large enough. These investigations pave the way for studying autocatalytic cycles with more complicated coupling, such as mutual catalysis.

Stochastic parabolic growth promotes coexistence and a relaxed error threshold in RNA-like replicator populations.

The RNA world hypothesis proposes that during the early evolution of life, primordial genomes of the first self-propagating evolutionary units existed in the form of RNA-like polymers. Autonomous, non-enzymatic, and sustained replication of such information carriers presents a problem, because product formation and hybridization between template and copy strands reduces replication speed. Kinetics of growth is then parabolic with the benefit of entailing competitive coexistence, thereby maintaining diversity. Here, we test the information-maintaining ability of parabolic growth in stochastic multispecies population models under the constraints of constant total population size and chemostat conditions. We find that large population sizes and small differences in the replication rates favor the stable coexistence of the vast majority of replicator species ('genes'), while the error threshold problem is alleviated relative to exponential amplification. In addition, sequence properties (GC content) and the strength of resource competition mediated by the rate of resource inflow determine the number of coexisting variants, suggesting that fluctuations in building block availability favored repeated cycles of exploration and exploitation. Stochastic parabolic growth could thus have played a pivotal role in preserving viable sequences generated by random abiotic synthesis and providing diverse genetic raw material to the early evolution of functional ribozymes.

All living things use molecules known as nucleic acids to store instructions on how to grow and maintain themselves and pass these instructions down to the next generation. However, it remains unclear how these systems may have evolved from simple molecules in the environment when life began over 3.6 billion years ago. One idea proposes that, before the first cells evolved, abiotic chemical processes gave rise to substantial building blocks of ribonucleic acids (or RNAs, for short). Over time, RNAs could have combined to form polymers of random sequences that started to copy themselves to make simple machines, only carrying the information required to make more of the same RNAs. Later on, these RNA molecules teamed up with proteins, fats and other molecules to make the first cells. When RNA replicates, the parent molecule is used as a template to assemble a new copy. While the new RNA molecule remains attached to its template it prevents the template being used to make more RNA. Therefore, it is thought that the speed at which a specific RNA machine copied itself may have varied in a pattern known as parabolic growth. Furthermore, when RNA replicates without the help of other biological molecules, the process is very prone to errors, which would have severely limited how much information the RNA machines were able to pass on to the next generation. Theoretical work suggested that under certain conditions, parabolic growth may favor the maintenance of a large amount of RNA sequence-coded information, but it is not clear if this is actually possible in nature. To address this question, Paczkó et al. developed mathematical models to investigate the effect of parabolic growth on the ability of RNA to replicate without other biological molecules. The models show that when large numbers of RNAs are present, small differences in how quickly different RNAs replicated favored the stable coexistence of different RNA sequences. Parabolic growth decreased the adverse effect of copying errors, allowing larger pieces of RNA to faithfully replicate themselves. This work suggests that parabolic growth may help to maintain different types of RNA (or similar replicating molecules) in a population and in turn, help new simple life forms to evolve. In the future, these findings may be used as a framework for laboratory experiments to better understand how early life forms may have evolved.

A neural network-based model framework for cell-fate decisions and development.

Gene regulatory networks (GRNs) fulfill the essential function of maintaining the stability of cellular differentiation states by sustaining lineage-specific gene expression, while driving the progression of development. However, accounting for the relative stability of intermediate differentiation stages and their divergent trajectories remains a major challenge for models of developmental biology. Here, we develop an empirical data-based associative GRN model (AGRN) in which regulatory networks store multilineage stage-specific gene expression profiles as associative memory patterns. These networks are capable of responding to multiple instructive signals and, depending on signal timing and identity, can dynamically drive the differentiation of multipotent cells toward different cell state attractors. The AGRN dynamics can thus generate diverse lineage-committed cell populations in a robust yet flexible manner, providing an attractor-based explanation for signal-driven cell fate decisions during differentiation and offering a readily generalizable modelling tool that can be applied to a wide variety of cell specification systems.

Small-molecule autocatalysis drives compartment growth, competition and reproduction.

Sustained autocatalysis coupled to compartment growth and division is a key step in the origin of life, but an experimental demonstration of this phenomenon in an artificial system has previously proven elusive. We show that autocatalytic reactions within compartments-when autocatalysis, and reactant and solvent exchange outpace product exchange-drive osmosis and diffusion, resulting in compartment growth. We demonstrate, using the formose reaction compartmentalized in aqueous droplets in an emulsion, that compartment volume can more than double. Competition for a common reactant (formaldehyde) causes variation in droplet growth rate based on the composition of the surrounding droplets. These growth rate variations are partially transmitted after selective division of the largest droplets by shearing, which converts growth-rate differences into differences in droplet frequency. This shows how a combination of properties of living systems (growth, division, variation, competition, rudimentary heredity and selection) can arise from simple physical-chemical processes and may have paved the way for the emergence of evolution by natural selection.

Directional selection coupled with kin selection favors the establishment of senescence.

BACKGROUND: Conventional wisdom in evolutionary theory considers aging as a non-selected byproduct of natural selection. Based on this, conviction aging was regarded as an inevitable phenomenon. It was also thought that in the wild organisms tend to die from diseases, predation and other accidents before they could reach the time when senescence takes its course. Evidence has accumulated, however, that aging is not inevitable and there are organisms that show negative aging even. Furthermore, old age does play a role in the deaths of many different organisms in the wild also. The hypothesis of programmed aging posits that a limited lifespan can evolve as an adaptation (i.e., positively selected for) in its own right, partly because it can enhance evolvability by eliminating "outdated" genotypes. A major shortcoming of this idea is that non-aging sexual individuals that fail to pay the demographic cost of aging would be able to steal good genes by recombination from aging ones. RESULTS: Here, we show by a spatially explicit, individual-based simulation model that aging can positively be selected for if a sufficient degree of kin selection complements directional selection. Under such conditions, senescence enhances evolvability because the rate of aging and the rate of recombination play complementary roles. The selected aging rate is highest at zero recombination (clonal reproduction). In our model, increasing extrinsic mortality favors evolved aging by making up free space, thereby decreasing competition and increasing drift, even when selection is stabilizing and the level of aging is set by mutation-selection balance. Importantly, higher extrinsic mortality is not a substitute for evolved aging under directional selection either. Reduction of relatedness decreases the evolved level of aging; chance relatedness favors non-aging genotypes. The applicability of our results depends on empirical values of directional and kin selection in the wild. CONCLUSIONS: We found that aging can positively be selected for in a spatially explicit population model when sufficiently strong directional and kin selection prevail, even if reproduction is sexual. The view that there is a conceptual link between giving up clonal reproduction and evolving an aging genotype is supported by computational results.

Modeling the origin of cells.

Protocells (dividing supramolecular vesicles harboring unlinked genetic replicators) are thought to have played an important role in the origin and early evolution of life. Under what scenario did such reproducers come into play? New work by Babajanyan et al. provides theoretical insight into the symbiosis between replicators and reproducing compartments.

Search and insight processes in card sorting games.

Insight problems are particularly interesting, because problems which require restructuring allow researchers to investigate the underpinnings of the Aha-experience, creativity and out of the box thinking. There is a need for new insight tasks to probe and extend the limits of existing theories and cognitive frameworks. To shed more light on this fascinating issue, we addressed the question: Is it possible to convey a well-known card sorting game into an insight task? We introduced different conditions and tested them via two online experiments (N = 546). Between the conditions we systematically varied the available perceptual features, and the existence of non-obvious rules. We found that our card sorting game elicited insight experience. In the first experiment, our data revealed that solution strategies and insight experience varied by the availability and saliency of perceptual features. The discovery of a non-obvious rule, which is not hinted at by perceptual features, was most difficult. With our new paradigm, we were able to construe ambiguous problems which allowed participants to find more than one solution strategy. Interestingly, we realized interindividual preferences for different strategies. The same problem drove strategies which either relied on feature integration or on more deliberate strategies. The second experiment varied the degree of independence of a sorting rule from the standard rules which were in accordance with prior knowledge. It was shown that the more independent the hidden rule was, the more difficult the task became. In sum, we demonstrated a new insight task which extended the available task domains and shed light on sequential and multi-step rule learning problems. Finally, we provided a first sketch of a cognitive model that should help to integrate the data within the existing literature on cognitive models and speculated about the generalizability of the interplay of prior knowledge modification and variation for problem solving.

Evolutionary ecology of language origins through confrontational scavenging.

A dynamic model and an agent-based simulation model implementing the assumptions of the confrontational scavenging hypothesis on early protolanguage as an adaptive response of Homo erectus to gradual change in their habitat has been developed and studied. The core assumptions of the hypothesis and the model scenario are the pre-adaptation of our ancestors to occupy the ecological niche that they constructed for themselves by having evolved displaced communication and a rudimentary tool manufacture, two features allowing them to use a new, concentrated and abundant resource-megafauna carrion-on the savannahs replacing arboreal habitats owing to the drying climate of East Africa at about 2 Ma. The shift in diet required coordinated cooperation by the hominin scavengers confronted with concurrent predators. Power scavenging compelled displaced symbolic communication featuring a limited semantic range; syntax was not yet required. We show that phenotypic evolution on the accuracy of information transfer between cooperating hominins is a necessary and sufficient condition for the population of agents to survive the diet shift. Both the individual and the group fitness of the hominin horde increased with the accuracy of their protolanguage, with decreasing time allocated to foraging and thus more time left for culture. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Human socio-cultural evolution in light of evolutionary transitions: introduction to the theme issue.

Human societies are no doubt complex. They are characterized by division of labour, multiple hierarchies, intricate communication networks and transport systems. These phenomena and others have led scholars to propose that human society may be, or may become, a new hierarchical level that may dominate the individual humans within it, similar to the relations between an organism and its cells, or an ant colony and its members. Recent discussions of the possibility of this major evolutionary transition in individuality (ETI) raise interesting and controversial questions that are explored in the present issue from four different complementary perspectives. (i) The general theory of ETIs. (ii) The unique aspects of cultural evolution. (iii) The evolutionary history and pre-history of humans. (iv) Specific routes of a possible human ETI. Each perspective uses different tools provided by different disciplines: biology, anthropology, cultural evolution, systems theory, psychology, economy, linguistics and philosophy of science. Altogether, this issue provides a broad and rich application of the notion of ETI to human past, present and perhaps also future evolution. It presents important case studies, new theoretical results and novel questions for future research. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Bayes and Darwin: How replicator populations implement Bayesian computations.

Bayesian learning theory and evolutionary theory both formalize adaptive competition dynamics in possibly high-dimensional, varying, and noisy environments. What do they have in common and how do they differ? In this paper, we discuss structural and dynamical analogies and their limits, both at a computational and an algorithmic-mechanical level. We point out mathematical equivalences between their basic dynamical equations, generalizing the isomorphism between Bayesian update and replicator dynamics. We discuss how these mechanisms provide analogous answers to the challenge of adapting to stochastically changing environments at multiple timescales. We elucidate an algorithmic equivalence between a sampling approximation, particle filters, and the Wright-Fisher model of population genetics. These equivalences suggest that the frequency distribution of types in replicator populations optimally encodes regularities of a stochastic environment to predict future environments, without invoking the known mechanisms of multilevel selection and evolvability. A unified view of the theories of learning and evolution comes in sight.

Novelty and imitation within the brain: a Darwinian neurodynamic approach to combinatorial problems.

Efficient search in vast combinatorial spaces, such as those of possible action sequences, linguistic structures, or causal explanations, is an essential component of intelligence. Is there any computational domain that is flexible enough to provide solutions to such diverse problems and can be robustly implemented over neural substrates? Based on previous accounts, we propose that a Darwinian process, operating over sequential cycles of imperfect copying and selection of neural informational patterns, is a promising candidate. Here we implement imperfect information copying through one reservoir computing unit teaching another. Teacher and learner roles are assigned dynamically based on evaluation of the readout signal. We demonstrate that the emerging Darwinian population of readout activity patterns is capable of maintaining and continually improving upon existing solutions over rugged combinatorial reward landscapes. We also demonstrate the existence of a sharp error threshold, a neural noise level beyond which information accumulated by an evolutionary process cannot be maintained. We introduce a novel analysis method, neural phylogenies, that displays the unfolding of the neural-evolutionary process.

Phenotypes to remember: Evolutionary developmental memory capacity and robustness.

There is increased awareness of the possibility of developmental memories resulting from evolutionary learning. Genetic regulatory and neural networks can be modelled by analogous formalism raising the important question of productive analogies in principles, processes and performance. We investigate the formation and persistence of various developmental memories of past phenotypes asking how the number of remembered past phenotypes scales with network size, to what extent memories stored form by Hebbian-like rules, and how robust these developmental "devo-engrams" are against networks perturbations (graceful degradation). The analogy between neural and genetic regulatory networks is not superficial in that it allows knowledge transfer between fields that used to be developed separately from each other. Known examples of spectacular phenotypic radiations could partly be accounted for in such terms.

Evolution of linkage and genome expansion in protocells: The origin of chromosomes.

Chromosomes are likely to have assembled from unlinked genes in early evolution. Genetic linkage reduces the assortment load and intragenomic conflict in reproducing protocell models to the extent that chromosomes can go to fixation even if chromosomes suffer from a replicative disadvantage, relative to unlinked genes, proportional to their length. Here we numerically show that chromosomes spread within protocells even if recurrent deleterious mutations affecting replicating genes (as ribozymes) are considered. Dosage effect selects for optimal genomic composition within protocells that carries over to the genic composition of emerging chromosomes. Lacking an accurate segregation mechanism, protocells continue to benefit from the stochastic corrector principle (group selection of early replicators), but now at the chromosome level. A remarkable feature of this process is the appearance of multigene families (in optimal genic proportions) on chromosomes. An added benefit of chromosome formation is an increase in the selectively maintainable genome size (number of different genes), primarily due to the marked reduction of the assortment load. The establishment of chromosomes is under strong positive selection in protocells harboring unlinked genes. The error threshold of replication is raised to higher genome size by linkage due to the fact that deleterious mutations affecting protocells metabolism (hence fitness) show antagonistic (diminishing return) epistasis. This result strengthens the established benefit conferred by chromosomes on protocells allowing for the fixation of highly specific and efficient enzymes.

From self-replication to replicator systems en route to de novo life.

The process by which chemistry can give rise to biology remains one of the biggest mysteries in contemporary science. The de novo synthesis and origin of life both require the functional integration of three key characteristics - replication, metabolism and compartmentalization - into a system that is maintained out of equilibrium and is capable of open-ended Darwinian evolution. This Review takes systems of self-replicating molecules as starting points and describes the steps necessary to integrate additional characteristics of life. We analyse how far experimental self-replicators have come in terms of Darwinian evolution. We also cover models of replicator communities that attempt to solve Eigen's paradox, whereby accurate replication needs complex machinery yet obtaining such complex self-replicators through evolution requires accurate replication. Successful models rely on a collective metabolism and a way of (transient) compartmentalization, suggesting that the invention and integration of these two characteristics is driven by evolution. Despite our growing knowledge, there remain numerous key challenges that may be addressed by a combined theoretical and experimental approach.

Encoding Temporal Regularities and Information Copying in Hippocampal Circuits.

Discriminating, extracting and encoding temporal regularities is a critical requirement in the brain, relevant to sensory-motor processing and learning. However, the cellular mechanisms responsible remain enigmatic; for example, whether such abilities require specific, elaborately organized neural networks or arise from more fundamental, inherent properties of neurons. Here, using multi-electrode array technology, and focusing on interval learning, we demonstrate that sparse reconstituted rat hippocampal neural circuits are intrinsically capable of encoding and storing sub-second-order time intervals for over an hour timescale, represented in changes in the spatial-temporal architecture of firing relationships among populations of neurons. This learning is accompanied by increases in mutual information and transfer entropy, formal measures related to information storage and flow. Moreover, temporal relationships derived from previously trained circuits can act as templates for copying intervals into untrained networks, suggesting the possibility of circuit-to-circuit information transfer. Our findings illustrate that dynamic encoding and stable copying of temporal relationships are fundamental properties of simple in vitro networks, with general significance for understanding elemental principles of information processing, storage and replication.

Multilevel selection as Bayesian inference, major transitions in individuality as structure learning.

Complexity of life forms on the Earth has increased tremendously, primarily driven by subsequent evolutionary transitions in individuality, a mechanism in which units formerly being capable of independent replication combine to form higher-level evolutionary units. Although this process has been likened to the recursive combination of pre-adapted sub-solutions in the framework of learning theory, no general mathematical formalization of this analogy has been provided yet. Here we show, building on former results connecting replicator dynamics and Bayesian update, that (i) evolution of a hierarchical population under multilevel selection is equivalent to Bayesian inference in hierarchical Bayesian models and (ii) evolutionary transitions in individuality, driven by synergistic fitness interactions, is equivalent to learning the structure of hierarchical models via Bayesian model comparison. These correspondences support a learning theory-oriented narrative of evolutionary complexification: the complexity and depth of the hierarchical structure of individuality mirror the amount and complexity of data that have been integrated about the environment through the course of evolutionary history.

Moderate sex between protocells can balance between a decrease in assortment load and an increase in parasite spread.

Sexual reproduction is widespread in nature despite the different kinds of cost that it entails. We do not know exactly when the first sexual process took place and especially why it was beneficial at first. It is clearer why sex is advantageous for the prokaryotes and eukaryotes but the benefit of sex for protocells with individually replicating ribozymes is not yet fully understood. In this context sex is the simple horizontal gene transfer among two protocells that undergo transient fusion. Many authors argue that horizontal gene transfer (HGT) was very common in the early stage of evolution. However, HGT is a risky mechanism considering both the disruption of optimal compositions and the spread of parasites among protocells. In order to test the effects of HGT on the fitness of a protocell population, we explored by numerical simulations those conditions under which fusion might have been beneficial. We investigated multiple conceivable types of fusion in the stochastic corrector model framework and we considered the spread of parasites in every case. Protocells contain up to five species of unlinked, essential ribozymes; if a protocell has the same amount of each, it reaches maximum fitness. Fusion is dangerous not only due to the spread of parasites but also because it can ruin the cells with balanced ribozyme composition. We show that fusion can restore the ribozyme composition of the protocells under certain circumstances (high gene count, intermediate split size and low rate of fusion) and thus it can decrease the effect of the genetic load. Fusion could have been a useful early mechanism in contributing to the reliable coexistence of the different ribozymes before the spread of the chromosomes.